Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-28T13:48:39.275Z Has data issue: false hasContentIssue false
  • English
  • Français

Cyclic variations in incubation conditions induce adaptive responses to later heat exposure in chickens: a review

Published online by Cambridge University Press:  14 August 2014

T. Loyau ,
L. Bedrani ,
C. Berri ,
S. Métayer-Coustard ,
C. Praud ,
V. Coustham ,
S. Mignon-Grasteau ,
M. J. Duclos ,
S. Tesseraud  and
N. Rideau
...Show all authors
T. Loyau
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
L. Bedrani
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
C. Berri
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
S. Métayer-Coustard
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
C. Praud
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
V. Coustham
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
S. Mignon-Grasteau
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
M. J. Duclos
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
S. Tesseraud
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
N. Rideau
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
C. Hennequet-Antier
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
N. Everaert
Affiliation:
KU Leuven, Department of Biosystems, Kasteelpark Arenberg 30, 3001 Leuven, Belgium University of Liège, Gembloux Agro-Bio Tech, Animal Science Unit, Passage des Déportés 2, 5030 Gembloux, Belgium
S. Yahav
Affiliation:
The Volcani Center, Institute of Animal Science, Bet Dagan P.O. Box 6, 50250, Israel.
A. Collin*
Affiliation:
INRA, UR83 Recherches Avicoles, F-37380 Nouzilly, France
*
†E-mail: [email protected]
Get access

Abstract

Selection programs have enabled broiler chickens to gain muscle mass without similar enlargement of the cardiovascular and respiratory systems that are essential for thermoregulatory efficiency. Meat-type chickens cope with high ambient temperature by reducing feed intake and growth during chronic and moderate heat exposure. In case of acute heat exposure, a dramatic increase in morbidity and mortality can occur. In order to alleviate heat stress in the long term, research has recently focused on early thermal manipulation. Aimed at stimulation of long-term thermotolerance, the thermal manipulation of embryos is a method based on fine tuning of incubation conditions, taking into account the level and duration of increases in temperature and relative humidity during a critical period of embryogenesis. The consequences of thermal manipulation on the performance and meat quality of broiler chickens have been explored to ensure the potential application of this strategy. The physiological basis of the method is the induction of epigenetic and metabolic mechanisms that control body temperature in the long term. Early thermal manipulation can enhance poultry resistance to environmental changes without much effect on growth performance. This review presents the main strategies of early heat exposure and the physiological concepts on which these methods were based. The cellular mechanisms potentially underlying the adaptive response are discussed as well as the potential interest of thermal manipulation of embryos for poultry production.

Keywords

thermal manipulationembryochickenheat exposurethermoregulation
Type
Research Article
Information
animal , Volume 9 , Issue 1 , January 2015 , pp. 76 - 85
Copyright
© The Animal Consortium 2014 

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.)

References

Altan, Ö, Altan, A, Çabuk, M and Bayraktar, H 2000. Effects of heat stress on some blood parameters in broilers. Turkish Journal of Veterinary Animal Science 24, 145–148.Google Scholar
Al-Zhgoul, MB, Dalab, AE, Ababneh, MM, Jawasreh, KI, Busadah, KA and Ismail, ZB 2013. Thermal manipulation during embryogenesis results in enhanced Hsp70 gene expression and the acquisition of thermotolerance. Research in Veterinary Science 95, 502–507.CrossRefGoogle Scholar
Arad, Z and Marder, J 1983. Acid-base regulation during thermal panting in the fowl (Gallus domesticus): comparison between breeds. Comparative Biochemistry and Physiology Part A: Physiology 74, 125–130.CrossRefGoogle ScholarPubMed
Boulant, JA 2006. Neuronal basis of Hammel’s model for set-point thermoregulation. Journal of Applied Physiology 100, 1347–1354.Google Scholar
Boussaid-Om Ezzine, S, Everaert, N, Metayer-Coustard, S, Rideau, N, Berri, C, Joubert, R, Temim, S, Collin, A and Tesseraud, S 2010. Effects of heat exposure on Akt/S6K1 signaling and expression of genes related to protein and energy metabolism in chicken (Gallus gallus) pectoralis major muscle. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 157, 281–287.Google Scholar
Bruzual, JJ, Peak, SD, Brake, J and Peebles, ED 2000. Effects of relative humidity during the last five days of incubation and brooding temperature on performance of broiler chicks from young broiler breeders. Poultry Science 79, 1385–1391.CrossRefGoogle ScholarPubMed
Collin, A, Picard, M and Yahav, S 2005. The effect of duration of thermal manipulation during broiler chick’s embryogenesis on body weight and body temperature of post hatched chicks. Animal Research 54, 105–112.Google Scholar
Collin, A, Bedrani, L, Loyau, T, Mignon-Grasteau, S, Metayer-Coustard, S, Praud, C, De Basilio, V, Requena Rodon, F, Bastianelli, D, Duclos, MJ, Tesseraud, S, Berri, C and Yahav, S 2011. Embryo acclimation: an innovative technique to limit mortality during thermal stress in chicken. INRA Productions Animales 24, 191–197.Google Scholar
Collin, A, Loyau, T, Bedrani, L, Berri, C, Métayer-Coustard, S, Praud, C, Duclos, MJ, Tesseraud, S, Rideau, N, Hennequet-Antier, C, Everaert, N, Mignon-Grasteau, S and Yahav, S 2012. Adaptive response of chickens to hot environments induced by changing incubation temperature. Proceedings of 24th World’s Poultry Congress, Bahia-Salvador, Brazil, 5–9 August, pp. 1–7.Google Scholar
Collin, A, Berri, C, Tesseraud, S, Requena, F, Cassy, S, Crochet, S, Duclos, MJ, Rideau, N, Tona, K, Buyse, J, Bruggeman, V, Decuypere, E, Picard, M and Yahav, S 2007. Effects of thermal manipulation during early and late embryogenesis on thermotolerance and breast muscle characteristics in broiler chickens. Poultry Science 86, 795–800.CrossRefGoogle ScholarPubMed
De Basilio, V and Picard, M 2002. La capacité de survie des poulets à un coup de chaleur est augmentée par une exposition précoce à une température élevée. INRA Productions Animales 15, 235–245.CrossRefGoogle Scholar
De Basilio, V, Vilariño, M, Yahav, S and Picard, M 2001. Early age thermal conditioning and a dual feeding program for male broilers challenged by heat stress. Poultry Science 80, 29–36.Google Scholar
De Basilio, V, Requena, F, León, A, Vilariño, M and Picard, M 2003. Early age thermal conditioning immediately reduces body temperature of broiler chicks in a tropical environment. Poultry Science 82, 1235–1241.Google Scholar
Debut, M, Berri, C, Arnould, C, Guémené, D, Santé-Lhoutellier, V, Sellier, N, Baéza, E, Jehl, N, Jégo, Y, Beaumont, C and Le Bihan-Duval, E 2005. Behavioural and physiological responses of three chicken breeds to preslaughter shackling and acute heat stress. British Poultry Science 46, 527–535.Google Scholar
Druyan, S, Piestun, Y and Yahav, S 2012. Heat stress in domestic fowl: genetic and physiological aspects. In Heat stress: causes, treatment and prevention (ed. S Josipovic and E Ludwig), pp. 1–30. Nova Science Publishers Inc., New York, NY, USA.Google Scholar
Geraert, PA, Padilha, JC and Guillaumin, S 1996a. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: growth performance, body composition and energy retention. The British Journal of Nutrition 75, 195–204.Google ScholarPubMed
Geraert, PA, Padilha, JC and Guillaumin, S 1996b. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: biological and endocrinological variables. The British Journal of Nutrition 75, 205–216.Google Scholar
Giloh, M, Shinder, D and Yahav, S 2012. Skin surface temperature of broiler chickens is correlated to body core temperature and indicative of the chicken’s thermoregulatory status. Poultry Science 91, 175–188.Google Scholar
Halevy, O, Krispin, A, Leshem, Y, McMurtry, JP and Yahav, S 2001. Early-age heat exposure affects skeletal muscle satellite cell proliferation and differentiation in chicks. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 281, 302–309.CrossRefGoogle ScholarPubMed
Havenstein, GB, Ferket, PR and Qureshi, MA 2003. Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82, 1509–1518.Google Scholar
Iqbal, A, Decuypere, E, Abd El Azim, A and Kühn, ER 1990. Pre- and post-hatch high temperature exposure affects the thyroid hormones and corticosterone response to acute heat stress in growing chicken (Gallus domesticus). Journal of Thermal Biology 15, 149–153.Google Scholar
Janke, O and Tzschentke, B 2010. Long-lasting effect of changes in incubation temperature on heat stress induced neuronal hypothalamic c-Fos expression in chickens. The Open Ornithology Journal 3, Special Issue: Early development and epigenetic programming of body functions in birds 150–155.CrossRefGoogle Scholar
Janke, O, Tzschentke, B, Höchel, J and Nichelmann, M 2002. Metabolic responses of chicken and Muscovy duck embryos to high incubation temperatures. Comparative Biochemistry Physiology A: Comparative Physiology 131, 741–750.Google Scholar
Kisliouk, T and Meiri, N 2009. A critical role for dynamic changes in histone H3 methylation at the BDNF promoter during postnatal thermotolerance acquisition. The European Journal of Neuroscience 30, 1909–1922.Google Scholar
Klandorf, H, Sharp, PJ and Macleod, MG 1981. The relationship between heat production and concentrations of plasma thyroid hormones in the domestic hen. General and Comparative Endocrinology 45, 513–520.Google Scholar
Leterrier, C, Colina, Y, Collin, A, Bastianelli, D, Constantin, P and De Basilio, V 2009. Effets d'élévations tardives de la température ambiante sur la température corporelle et l'hyperventilation chez le poulet. Proceedings of the 8èmes Journées de la Recherche Avicole, St-Malo, France, 25–26 March, pp. 90–94.Google Scholar
Loyau, T, Berri, C, Bedrani, L, Métayer-Coustard, S, Praud, C, Duclos, MJ, Tesseraud, S, Rideau, N, Baéza, E, Chartrin, P, Hennequet-Antier, C, Everaert, N, Yahav, S, Mignon-Grasteau, S and Collin, A 2013. Embryo thermal manipulations modifies the physiology and body compositions of broiler chickens reared in floor pens without altering breast meat processing quality. Journal of Animal Science 91, 3674–3685.Google Scholar
Lozano, C, De Basilio, V, Oliveros, I, Alvarez, R, Colina, I, Bastianelli, D, Yahav, S and Picard, M 2006. Is sequential feeding a suitable technique to compensate for the negative effects of a tropical climate in finishing broilers? Animal Research 55, 71–76.Google Scholar
Molenaar, R, Hulet, R, Meijerhof, R, Maatjens, CM, Kemp, B and van den Brand, H 2011. High eggshell temperatures during incubation decrease growth performance and increase the incidence of ascites in broiler chickens. Poultry Science 90, 624–632.Google Scholar
Moraes, VMB, Malheiros, RD, Bruggeman, V, Collin, A, Tona, K, Van As, P, Onagbesan, OM, Buyse, J, Decuypere, E and Macari, M 2003. Effect of thermal conditioning during embryonic development on aspects of physiological responses of broilers to heat stress. Journal of Thermal Biology 28, 133–140.Google Scholar
Moraes, VMB, Malheiros, RD, Bruggeman, V, Collin, A, Tona, K, Van As, P, Onagbesan, OM, Buyse, J, Decuypere, E and Macari, M 2004. The effect of timing of thermal conditioning during incubation on embryo physiological parameters and its relationship to thermotolerance in adult broiler chickens. Journal of Thermal Biology 29, 55–61.Google Scholar
Mujahid, A, Yoshiki, Y, Akiba, Y and Toyomizu, M 2005. Superoxide radical production in chicken skeletal muscle induced by acute heat stress. Poultry Science 84, 307–314.CrossRefGoogle ScholarPubMed
Piestun, Y, Halevy, O and Yahav, S 2009a. Thermal manipulations of broiler embryos, the effect on thermoregulation and development during embryogenesis. Poultry Science 88, 2677–2688.Google Scholar
Piestun, Y, Zimmerman, I and Yahav, S 2013b. Pre-natal thermal manipulation of turkey embryos-effects on embryo development and post-hatch performances. Proceedings of WPSA Workshop Incubation and Fertility Research Group meeting, Göttingen, Germany, 31 September–1 October, p. 2.Google Scholar
Piestun, Y, Druyan, S, Brake, J and Yahav, S 2013a. Thermal manipulations during broiler incubation alters performance of broilers to 70 days of age. Poultry Science 92, 1155–1163.CrossRefGoogle ScholarPubMed
Piestun, Y, Harel, M, Barak, M, Yahav, S and Halevy, O 2009b. Thermal manipulations in late-term chick embryos have immediate and longer term effects on myoblast proliferation and skeletal muscle hypertrophy. Journal of Applied Physiology 106, 233–240.CrossRefGoogle ScholarPubMed
Piestun, Y, Shinder, D, Ruzal, M, Halevy, O, Brake, J and Yahav, S 2008. Thermal manipulations in late-term chick embryos have immediate and longer term effects on myoblast proliferation and skeletal muscle hypertrophy. Poultry Science 87, 1516–1525.Google Scholar
Piestun, Y, Halevy, O, Shinder, D, Ruzal, M, Druyan, S and Yahav, S 2011. Thermal manipulations during broiler embryogenesis improves post-hatch performance under hot conditions. Journal of Thermal Biology 36, 469–474.CrossRefGoogle Scholar
Pinchuck, S, Meiri, N and Yahav, S 2011. The effect of thermal manipulation, during early embryogenesis, on angiogenesis and thermo-tolerance in broilers. Proceedings of WPSA Workshop Fundamental Physiology and Perinatal Development in Poultry, Wageningen, The Netherlands, 31 August–3 September, pp. 44–45.Google Scholar
Renaudeau, D, Collin, A, Yahav, S, de Basilio, V, Gourdine, JL and Collier, RJ 2012. Adaptation to tropical climate and strategies to alleviate heat stress in livestock production. Animal 6, 707–728.Google Scholar
Sandercock, DA, Hunter, RR, Mitchell, MA and Hocking, PM 2006. Thermoregulatory capacity and muscle membrane integrity are compromised in broilers compared with layers at the same age or body weight. British Poultry Science 47, 322–329.CrossRefGoogle ScholarPubMed
Taouis, M, De Basilio, V, Mignon-Grasteau, S, Crochet, S, Bouchot, C, Bigot, K, Collin, A and Picard, M 2002. Early-age thermal conditioning reduces uncoupling protein messenger RNA expression in pectoral muscle of broiler chicks at seven days of age. Poultry Science 81, 1640–1643.Google Scholar
Temim, S, Bedrani, L, Ain Baziz, H, Ghaoui, H, Boudina, H, Adjou, K, Collin, A and Tesseraud, S 2009. Effets de l’acclimatation précoce sur les performances de croissance et la morphométrie intestinale des poulets de chair élevés en conditions estivales méditerranéennes. European Journal of Scientific Research 38, 110–118.Google Scholar
Tesseraud, S and Temim, S 1999. Modifications métaboliques chez le poulet de chair en climat chaud: conséquences nutritionnelles. INRA Productions Animales 12, 353–363.CrossRefGoogle Scholar
Tona, K, Onagbesan, O, Bruggeman, V, Collin, A, Berri, C, Duclos, M, Tesseraud, S, Buyse, J, Decuypere, E and Yahav, S 2008. Effects of heat conditioning at d 16 to 18 of incubation or during early broiler rearing on embryo physiology, post-hatch growth performance and heat tolerance. Archiv für Geflügelkunde 72, 75–83.Google Scholar
Tzschentke, B and Basta, D 2002. Early development of neuronal hypothalamic thermosensivity in birds: influence of epigenetic temperature adaptation. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 131, 825–832.Google Scholar
Tzschentke, B and Halle, I 2009. Influence of temperature stimulation during the last 4 days of incubation on secondary sex ratio and later performance male and female broiler chickens. British Poultry Science 50, 634–640.Google Scholar
Uni, Z, Gal-Garber, O, Geyra, A, Sklan, D and Yahav, S 2001. Changes in growth and function of chick small intestine epithelium due to early thermal conditioning. Poultry Science 80, 438–445.Google Scholar
Walstra, I, Ten Napel, J, Kemp, B and Van Den Brand, H 2010. Temperature manipulation during layer chick embryogenesis. Poultry Science 89, 1502–1508.Google Scholar
Whittow, GC, Sturkie, PD and Stein, G 1964. Cardiovascular changes associated with thermal polypnea in the chicken. American Journal of Physiology 207, 1349–1353.CrossRefGoogle ScholarPubMed
Willemsen, H, Kamers, B, Dahlke, F, Han, H, Song, Z, Ansari Pirsaraei, Z, Tona, K, Decuypere, E and Everaert, N 2010. High-and low-temperature manipulation during late incubation: effects on embryonic development, the hatching process, and metabolism in broilers. Poultry Science 89, 2678–2690.Google Scholar
Wolfenson, D 1986. The effect of acclimatization on blood flow and its distribution in normothermic and hyperthermic domestic fowl. Comparative Biochemistry and Physiology. Part A, Comparative Physiology 85, 739–742.CrossRefGoogle ScholarPubMed
Yahav, S 2009. Alleviating heat stress in domestic fowl – different strategies. World’s Poultry Science Journal 65, 719–732.Google 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.CrossRefGoogle ScholarPubMed
Yahav, S and McMurtry, JP 2001. Thermotolerance acquisition in broiler chickens by temperature conditioning early in life – the effect of timing and ambient temperature. Poultry Science 80, 1662–1666.Google Scholar
Yahav, S, Sasson-Rath, R and Shinder, D 2004b. 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.Google Scholar
Yahav, S, Straschnow, A, Plavnik, I and Hurwitz, S 1997. Blood system response of chickens to changes in environmental temperature. Poultry Science 76, 627–633.Google Scholar
Yahav, S, Collin, A, Shinder, D and Picard, M 2004a. Thermal manipulations during broiler chick’s embryogenesis, the effect of timing and temperature. Poultry Science 83, 1959–1963.CrossRefGoogle ScholarPubMed
Yahav, S, Shinder, D, Ruzal, M, Giloh, M and Piestun, Y 2009. Controlling body temperature – the opportunities for highly productive domestic fowl. In Body temperature control (ed. AB Cisneros and BL Goins), pp. 65–98. Nova Science Publishers Inc., New York, NY, USA.Google Scholar
Yalçin, S and Siegel, PB 2003. Developmental stability of broiler embryos in relation to length of egg storage prior to incubation. Journal of Poultry Science 40, 298–308.CrossRefGoogle Scholar
Yalçin, S, Özkan, S, Çabuk, M, Buyse, J, Decuypere, E and Siegel, PB 2005. Pre- and postnatal conditioning induced thermotolerance on body weight, physiological responses and relative asymmetry of broilers originating from young and old breeder flocks. Poultry Science 84, 967–976.Google Scholar
Yalçin, S, Cabuk, M, Bruggeman, V, Babacanoglu, E, Buyse, J, Decuypere, E and Siegel, PB 2008. Acclimation to heat during incubation: 3. Body weight, cloacal temperatures, and blood acid-base balance in broilers exposed to daily high temperatures. Poultry Science 87, 2671–2677.Google Scholar
Yossifoff, M, Kisliouk, T and Meiri, N 2008. Dynamic changes in DNA methylation during thermal control establishment affect CREB binding to the brain-derived neurotrophic factor promoter. European Journal of Neuroscience 28, 2267–2277.Google Scholar