Thermal manipulation of the embryo modifies the physiology and body composition of broiler chickens reared in floor pens without affecting breast meat processing quality.
Loyau, T.; Berri, C.; Bedrani, L.et al.
2013 • In Journal of Animal Science, 91 (8), p. 3674-85
body composition; broiler chicken; heat stress; meat quality; respiratory physiology; thermal manipulation of embryos
Abstract :
[en] Selection in broiler chickens has increased muscle mass without similar development of the cardiovascular and respiratory systems, resulting in limited ability to sustain high ambient temperatures. The aim of this study was to determine the long-lasting effects of heat manipulation of the embryo on the physiology, body temperature (Tb), growth rate and meat processing quality of broiler chickens reared in floor pens. Broiler chicken eggs were incubated in control conditions (37.8 degrees C, 56% relative humidity; RH) or exposed to thermal manipulation (TM; 12 h/d, 39.5 degrees C, 65% RH) from d 7 to 16 of embryogenesis. This study was planned in a pedigree design to identify possible heritable characters for further selection of broiler chickens to improve thermotolerance. Thermal manipulation did not affect hatchability but resulted in lower Tb at hatching and until d 28 post-hatch, with associated changes in plasma thyroid hormone concentrations. At d 34, chickens were exposed to a moderate heat challenge (5 h, 32 degrees C). Greater O2 saturation and reduced CO2 partial pressure were observed (P < 0.05) in the venous blood of TM than in that of control chickens, suggesting long-term respiratory adaptation. At slaughter age, TM chickens were 1.4% lighter and exhibited 8% less relative abdominal fat pad than controls. Breast muscle yield was enhanced by TM, especially in females, but without significant change in breast meat characteristics (pH, color, drip loss). Plasma glucose/insulin balance was affected (P < 0.05) by thermal treatments. The heat challenge increased the heterophil/lymphocyte ratio in controls (P < 0.05) but not in TM birds, possibly reflecting a lower stress status in TM chickens. Interestingly, broiler chickens had moderate heritability estimates for the plasma triiodothyronine/thyroxine concentration ratio at d 28 and comb temperature during the heat challenge on d 34 (h(2) > 0.17). In conclusion, TM of the embryo modified the physiology of broilers in the long term as a possible adaptation for heat tolerance, without affecting breast meat quality. This study highlights the value of 2 new heritable characters involved in thermoregulation for further broiler selection.
Disciplines :
Animal production & animal husbandry
Author, co-author :
Loyau, T.
Berri, C.
Bedrani, L.
Metayer-Coustard, S.
Praud, C.
Duclos, M. J.
Tesseraud, S.
Rideau, N.
Everaert, Nadia ; KU Leuven > Department of Biosystems > Division Livestock-Nutrition-Quality
Yahav, S.
Mignon-Grasteau, S.
Collin, A.
Language :
English
Title :
Thermal manipulation of the embryo modifies the physiology and body composition of broiler chickens reared in floor pens without affecting breast meat processing quality.
Publication date :
2013
Journal title :
Journal of Animal Science
ISSN :
0021-8812
eISSN :
1525-3163
Publisher :
American Society of Animal Science, United States - Illinois
Aksit, M., S. Yalçin, S. Ozkan, K. Metin, and D. Ozdemir. 2006. Effects of temperature during rearing and crating on stress parameters and meat quality of broilers. Poult. Sci. 85:1867-1874.
Altan, O., A. Altan, M. Cabuk, and H. Bayraktar. 2000. Effects of heat stress on some blood parameters in broilers. Turk. J. Vet. Anim. Sci. 24:145-148.
Altan, O., A. Pabuccuoglu, A. Altan, S. Konyalioglu, and H. Bayraktar. 2003. Effect of heat stress on oxidative stress, lipid peroxidation and some stress parameters in broilers. Br. Poult. Sci. 44:545-550.
Arad, Z., and J. Marder. 1983. Acid-base regulation during thermal panting in the fowl (gallus-domesticus)-comparison between breeds. Comp. Biochem. Physiol. A. Physiol. 74:125-130.
Athens, J.W. 1993. Variations of leukocytes in disease. In: G.R. Lee, T.C. Bithell, J. Foerster, J.W. Athens, J.W. Lukens, editors, Wintrobe's clinical hematology. 9th edition. Malvern, PA. Lea and Febiger, p. 1564.
Balnave, D., and I. Gorman. 1993. A role for sodium-bicarbonate supplements for growing broilers at high-temperatures. Worlds Poult. Sci. J. 49:236-241.
Berri, C., E. Le Bihan-Duval, M. Debut, V. Santé-Lhoutellier, E. Baéza, V. Gigaud, Y. Jégo, and M. J. Duclos. 2007. Consequence of muscle hypertrophy on characteristics of Pectoralis major muscle and breast meat quality of broiler chickens. J. Anim. Sci. 85:2005-2011.
Beuving, G. 1989. The effects of the laying nest on the corticosterone levels in the plasma of laying hens prior to oviposition. Tijdschr. Diergeneeskd. 114:3-9.
Borges, S.A., A.V. Fischer da Silva, J. Ariki, D.M. Hooge, and K.R. Cummings. 2003. Dietary electrolyte balance for broiler chickens exposed to thermoneutral or heat-stress environments. Poult. Sci. 82:428-435.
Boussaid-Om Ezzine, S., N. Everaert, S. Metayer-Coustard, N. Rideau, C. Berri, R. Joubert, S. Temim, A. Collin, and S. Tesseraud. 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. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 157:281-287.
Bruzual, J. J., S. D. Peak, J. Brake, and E. D. Peebles. 2000. Effects of relative humidity during the last five days of incubation and brooding temperature on performance of broiler chicks from young broiler breeders. Poult. Sci. 79:1385-1391.
Chartrin, P., M. D. Bernadet, G. Guy, J. Mourot, J. F. Hocquette, N. Rideau, M. J. Duclos, and E. Baeza. 2006. Does overfeeding enhance genotype effects on liver ability for lipogenesis and lipid secretion in ducks? Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 145:390-396.
Collin, A., L. Bedrani, T. Loyau, S. Mignon-Grasteau, S. Metayer-Coustard, C. Praud, C. Praud, V. De Basilio, F. Requena Rodon, D. Bastianelli, M. J. Duclos, S. Tesseraud, C. Berri, and S. Yahav. 2011. Lácclimatation embryonnaire: Une technique innovante pour limiter les mortalitées liées au stress thermique chez le poulet. INRA Prod. Anim. 24:191-198.
Collin, A., C. Berri, S. Tesseraud, F. E. R. Rodon, S. Skiba-Cassy, S. Crochet, M. J. Duclos, N. Rideau, K. Tona, J. Buyse, V. Bruggeman, E. Decuypere, M. Picard, and S. Yahav. 2007. Effects of thermal manipulation during early and late embryogenesis on thermotolerance and breast muscle characteristics in broiler chickens. Poult. Sci. 86:795-800.
Collin, A., J. Buyse, P. Van As, V. M. Darras, R. D. Malheiros, V. M. B. Moraes, G. E. Reyns, M. Taouis, and E. Decuypere. 2003. Cold-induced enhancement of avian uncoupling protein expression, heat production, and triiodothyronine concentrations in broiler chicks. Gen. Comp. Endocrinol. 130:70-77.
Collin, A., R. Joubert, Q. Swennen, M. Damon, S. Métayer Coustard, S. Skiba-Cassy, N. Everaert, J. Buyse, and S. Tesseraud. 2009. Involvement of thyroid hormones in the regulation of mitochondrial oxidations in mammals and birds. In Novascience, editor, Thyroid hormones: Functions, related diseases and uses. Kuehn F.S., Lozad M.P., New York.
Collin, A., M. Picard, and S. Yahav. 2005. The effect of duration of thermal manipulation during broiler chick embryogenesis on body weight and body temperature of post-hatched chicks. Anim. Res. 54:105-111.
Darras, V. M., S. P. Kotanen, K. L. Geris, L. R. Berghman, and E. R. Kuhn. 1996. Plasma thyroid hormone levels and iodothyronine deiodinase activity following an acute glucocorticoid challenge in embryonic compared with posthatch chickens. Gen. Comp. Endocrinol. 104:203-212.
Darras, V. M., C. H. Verhoelst, G. E. Reyns, E. R. Kühn, and S. Van der Geyten. 2006. Thyroid hormone deiodination in birds. Thyroid 16:25-35.
De Basilio, V., F. Requena, A. Leon, M. Vilarino, and M. Picard. 2003. Early age thermal conditioning immediately reduces body temperature of broiler chicks in a tropical environment. Poult. Sci. 82:1235-1241.
Debut, M., C. Berri, C. Arnould, D. Guemene, V. Sante-Lhoutellier, N. Sellier, E. Baeza, N. Jehl, Y. Jego, C. Beaumont, and E. Le Bihan-Duval. 2005. Behavioural and physiological responses of three chicken breeds to pre-slaughter shackling and acute heat stress. Br. Poult. Sci. 46:527-535.
Decuypere, E. 1984. Incubation-temperature in relation to postnatal performance in chickens. Arch. Exp. Veterinarmed. 38:439-449.
Druyan, S., Y. Piestun, and S. Yahav. 2012. Heat stress in domestic fowl-genetic and physiological aspects. In S. Josipovic and E. Ludwig, editors, Heat stress-causes, treatment and prevention. NovaScience publications Inc, New York.
Geraert, P.A., J.C.F. Padilha, and S. Guillaumin. 1996. Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: Growth performance, body composition and energy retention. Br. J. Nutr. 75:195-204.
Giloh, M., D. Shinder, and S. Yahav. 2012. Skin surface temperature of broiler chickens is correlated to body core temperature and is indicative of their thermoregulatory status. Poult. Sci. 91:175-188.
Groeneveld, E., M. Kovac, and N. Menlenz. 2010. VCE6 User's guide and reference manual, Neustadt, Germany: Institute of animal husbandry and animal behaviour.
Gross, W. B., and P. B. Siegel. 1980. Effects of early environmental stresses on chicken body-weight, antibody-response to rbc antigens, feed-efficiency, and response to fasting. Avian Dis. 24:569-579.
Gross, W. B., and H. S. Siegel. 1983. Evaluation of the heterophil lymphocyte ratio as a measure of stress in chickens. Avian Dis. 27:972-979.
Halevy, O., A. Krispin, Y. Leshem, J. P. McMurtry, and S. Yahav. 2001. Early-age heat exposure affects skeletal muscle satellite cell proliferation and differentiation in chicks. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R302-R309.
Hammond, C. L., B. H. Simbi, and N. C. Stickland. 2007. In ovo temperature manipulation influences embryonic motility and growth of limb tissues in the chick (Gallus gallus). J. Exp. Biol. 210:2667-2675.
Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003a. Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1509-1518.
Havenstein, G. B., P. R. Ferket, and M. A. Qureshi. 2003b. Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1500-1508.
Iqbal, A., A. A. Elazim, E. Decuypere, and E. R. Kuhn. 1989. Prenatal and postnatal heat acclimation modulates thyroid and growthhormone response to acute heat-stress in the growing chicken. Gen. Comp. Endocrinol. 74:276.
Janke, O., B. Tzschentke, J. Hochel, and M. Nichelmann. 2002. Metabolic responses of chicken and muscovy duck embryos to high incubation temperatures. Comp. Biochem. Physiol. A. Mol. Integr. Physiol. 131:741-750.
Kornbrust, D. J., and R. D. Mavis. 1980. Relative susceptibility of microsomes from lung, heart, liver, kidney, brain and testes to lipidperoxidation-correlation with vitamin-e content. Lipids 15:315-322.
Le Bihan-Duval, E., C. Berri, E. Baeza, N. Millet, and C. Beaumont. 2001. Estimation of the genetic parameters of meat characteristics and of their genetic correlations with growth and body composition in an experimental broiler line. Poult. Sci. 80:839-843.
Le Bihan-Duval, E., M. Debut, C. M. Berri, N. Sellier, V. Sante-Lhoutellier, Y. Jego, and C. Beaumont. 2008. Chicken meat quality: Genetic variability and relationship with growth and muscle characteristics. BMC Genet. doi:10.1186/1471-2156-9-53.
Lin, H., E. Decuypere, and J. Buyse. 2006. Acute heat stress induces oxidative stress in broiler chickens. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 144:11-17.
Lynch, S. M., and B. Frei. 1993. Mechanisms of copper-dependent and iron-dependent oxidative modification of human low-density-lipoprotein. J. Lipid Res. 34:1745-1753.
Maxwell, M. H., G. W. Robertson, M. A. Mitchell, and A. J. Carlisle. 1992. The fine-structure of broiler chicken blood-cells, with particular reference to basophils, after severe heat-stress. Comp. Haematol. Int. 2:190-200.
Maxwell, M. H., G. W. Robertson, S. Spence, and C. C. McCorquodale. 1990. Comparison of haematological values in restricted-and ad libitum-fed domestic fowls: Red blood cell characteristics. Br. Poult. Sci. 31:407-413.
Minne, B., and E. Decuypere. 1984. Effects of late prenatal temperatures on some thermoregulatory aspects in young chickens. Arch. Exp. Veterinarmed. 38:374-383.
Moraes, V. M. B., R. D. Malheiros, V. Bruggeman, A. Collin, K. Tona, P. Van As, O. M. Onagbesan, J. Buyse, E. Decuypere, and M. Macari. 2003. Effect of thermal conditioning during embryonic development on aspects of physiological responses of broilers to heat stress. J. Therm. Biol. 28:133-140.
Moraes, V. M. B., R. D. Malheiros, V. Bruggeman, A. Collin, K. Tona, P. Van As, O. M. Onagbesan, J. Buyse, E. Decuypere, and M. Macari. 2004. The effect of timing of thermal conditioning during incubation on embryo physiological parameters and its relationship to thermotolerance in adult broiler chickens. J. Therm. Biol. 29:55-61.
Mujahid, A., Y. Akiba, C. H. Warden, and M. Toyomizu. 2007. Sequential changes in superoxide production, anion carriers and substrate oxidation in skeletal muscle mitochondria of heatstressed chickens. FEBS Lett. 581:3461-3467.
Nadaf, J., F. Pitel, H. Gilbert, M. J. Duclos, F. Vignoles, C. Beaumont, A. Vignal, T. E. Porter, L. A. Cogburn, S. E. Aggrey, J. Simon, and E. Le Bihan-Duval. 2009. QTL for several metabolic traits map to loci controlling growth and body composition in an F2 intercross between high-and low-growth chicken lines. Physiol. Genomics 38:241-249.
Nichelmann, M., B. Lange, R. Pirow, J.L. Langbein, and S. Herrmann. 1994. Avian thermoregulation during the perinal period. In E. Zeisberger, E. Schönbaum, and P. Lomax, editors, Thermal balance in health and diseases. Recent basic research and clinical progress. Birkhaüser, Basel, Switzerland. p. 167-173.
Piestun, Y., S. Druyan, J. Brake, and S. Yahav. 2013. Thermal manipulations during broiler incubation alters performance of broilers to 70 days of age. Poult. Sci. (in press).
Piestun, Y., O. Halevy, D. Shinder, M. Ruzal, S. Druyan, and S. Yahav. 2011. Thermal manipulations during broiler embryogenesis improves post-hatch performance under hot conditions. J. Therm. Biol. 36:469-474.
Piestun, Y., O. Halevy, and S. Yahav. 2009a. Thermal manipulations of broiler embryos-the effect on thermoregulation and development during embryogenesis. Poult. Sci. 88:2677-2688.
Piestun, Y., M. Harel, M. Barak, S. Yahav, and O. Halevy. 2009b. Thermal manipulations in late-term chick embryos have immediate and longer term effects on myoblast proliferation and skeletal muscle hypertrophy. J. Appl. Physiol. 106:233-240.
Piestun, Y., D. Shinder, M. Ruzal, O. Halevy, J. Brake, and S. Yahav. 2008. Thermal manipulations during broiler embryogenesis: Effect on the acquisition of thermotolerance. Poult. Sci. 87:1516-1525.
Prieto, M. T., and J. L. Campo. 2010. Effect of heat and several additives related to stress levels on fluctuating asymmetry, heterophil: Lymphocyte ratio, and tonic immobility duration in White Leghorn chicks. Poult. Sci. 89:2071-2077.
Rideau, N., and S. Métayer-Coustard. 2012. Utilisation périphérique du glucose chez le poulet et le canard: Implication pour la croissance et la qualité de la viande. INRA Prod. Anim. 25:337-350.
Ruffier, L., J. Simon, and N. Rideau. 1998. Isolation of functional glucagon islets of Langerhans from the chicken pancreas. Gen. Comp. Endocrinol. 112:153-162.
Sandercock, D. A., R. R. Hunter, M. A. Mitchell, and P. M. Hocking. 2006. Thermoregulatory capacity and muscle membrane integrity are compromised in broilers compared with layers at the same age or body weight. Br. Poult. Sci. 47:322-329.
Shinder, D., M. Ruzal, M. Giloh, S. Druyan, Y. Piestun, and S. Yahav. 2011. Improvement of cold resistance and performance of broilers by acute cold exposure during late embryogenesis. Poult. Sci. 90:633-641.
Smith, M. O., and R. G. Teeter. 1987. Effect of ammonium-chloride and kcl on survival of broiler chicks during acute heat-stress. Nutr. Res. 7:677-681.
Speake, B. K., A. M. B. Murray, and R. C. Noble. 1998. Transport and transformations of yolk lipids during development of the avian embryo. Prog. Lipid Res. 37:1-32.
Thonnard-Neumann, E. 1961. The Influence of hormones on the basophilic leukocytes. Acta Haematol. 25:261-270.
Tona, K., O. Onagbesan, V. Bruggeman, A. Collin, C. Berri, M. J. Duclos, S. Tesseraud, J. Buyse, E. Decuypere, and S. Yahav. 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. Arch. Geflugelkd. 72:75-83.
Tzschentke, B. 2007. Attainment of thermoregulation as affected by environmental factors. Poult. Sci. 86:1025-1036.
Tzschentke, B., and D. Basta. 2002. Early development of neuronal hypothalamic thermosensitivity in birds: Influence of epigenetic temperature adaptation. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 131:825-832.
Willemsen, H., Y. Li, E. Willems, L. Franssens, Y. Wang, E. Decuypere, and N. Everaert. 2011. Intermittent thermal manipulations of broiler embryos during late incubation and their immediate effect on the embryonic development and hatching process. Poult. Sci. 90:1302-1312.
Yahav, S. 2009. Alleviating heat stress in domestic fowl: Different strategies. Worlds Poult. Sci. J. 65:719-732.
Yahav, S., A. Collin, D. Shinder, and M. Picard. 2004a. Thermal manipulations during broiler chick embryogenesis: Effects of timing and temperature. Poult. Sci. 83:1959-1963.
Yahav, S., R. S. Rath, and D. Shinder. 2004b. The effect of thermal manipulations during embryogenesis of broiler chicks (Gallus domesticus) on hatchability, body weight and thermoregulation after hatch. J. Therm. Biol. 29:245-250.
Yahav, S., D. Shinder, J. Tanny, and S. Cohen. 2005. Sensible heat loss: The broiler's paradox. Worlds Poult. Sci. J. 61:419-434.
Yalçin, S., M. Cabuk, V. Bruggeman, E. Babacanoglu, J. Buyse, E. Decuypere, and P. B. Siegel. 2008. Acclimation to heat during incubation. 1. Embryonic morphological traits, blood biochemistry, and hatching performance. Poult. Sci. 87:1219-1228.
Zuidhof, M. J., F. E. Robinson, J. J. Feddes, R. T. Hardin, J. L. Wilson, R. I. McKay, and M. Newcombe. 1995. The effects of nutrient dilution on the well-being and performance of female broiler breeders. Poult. Sci. 74:441-456.
Zulkifli, I., A. Al-Aqil, A. R. Omar, A. Q. Sazili, and M. A. Rajion. 2009. Crating and heat stress influence blood parameters and heat shock protein 70 expression in broiler chickens showing short or long tonic immobility reactions. Poult. Sci. 88:471-476.