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Stress impairs the reproduction of laying hens: an involvement of energy

  • X.J. WANG (a1), L. LIU (a1), J.P. ZHAO (a1), H.C. JIAO (a1) and H. LIN (a1)...
Abstract

The reduction of reproductive performance associated with stress is a known phenomenon in domestic birds. This review demonstrates the involvement of glucocorticoids, a stress hormone, in the decision-making process regarding energy ingestion and distribution in laying hens. During the energetic challenge induced by a stressful environment, corticosterone stimulates energy intake and a preference for a high-fat diet by up-regulating neuropeptide Y (NPY) expression via the AMP-activated protein kinase (AMPK) pathway. The elevated corticosterone levels in response to stressors may be associated with suppressed reproduction in laying hens via a possible perturbation of the hypothalamic-pituitary-gonadal (HPG) axis. Corticosterone suppresses follicular development and is energy dependent by decreasing the availability of the circulating yolk precursor and the prevention of yolk deposition in follicles. Energy status is also involved in rejuvenation in moult hens.

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Corresponding author: hailin@sdau.edu.cn
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ARIYADI B., ISOBE N. and YOSHIMURA Y. (2012) Differences in the mucosal surface barrier formed by mucin in the lower oviductal segments between laying and molting hens. Poultry Science 91: 1173-1178.
ASTHEIMER L.B., BUTTEMER W.A. and WINGFIELD J.C. (1995) Seasonal and acute changes in adrenocortical responsiveness in an arctic-breeding bird. Hormones and Behavior 29: 442-457.
BALL G.F. (1993) The neural integration of environmental information by seasonally breeding birds. American Zoologist 33: 185-199.
BAMBINO T. and HSUEH A. (1981) Direct inhibitory effect of glucocorticoids upon testicular LH receptors and steroidogenesis in vivo and in vitro. Endocrinology 108: 2142-2147.
BARTOV I. (1985) Effects of dietary protein concentration and corticosterone injections on energy and nitrogen balances and fat deposition in broiler chicks. British Poultry Science 26: 311-324.
BERRY W.D. (2003) The physiology of induced molting. Poultry Science 82: 971-980.
BLAS J. (2015) Stress in birds, in: SCANES, C.G. (Eds) Sturkie's Avian Physiology, 6th, pp. 769-810 (London, Academic Press).
BLUNDELL J.E. and MACDIARMID J.I. (1997) Fat as a risk factor for overconsumption: satiation, satiety, and patterns of eating. Journal of the American Dietetic Association 97 (7 Suppl): S63-S69.
BRAKE J. and THAXTON P. (1979) Physiological changes in caged layers during a forced molt. 2. gross changes in organs. Poultry Science 58: 707-716.
CAI Y., SONG Z., ZHANG X., WANG X., JIAO H. and LIN H. (2009) Increased de novo lipogenesis in liver contributes to the augmented fat deposition in dexamethasone exposed broiler chickens (Gallus gallus domesticus). Comparative Biochemistry & Physiology Part C Toxicology & Pharmacology 150: 164-169.
CAI Y., SONG Z., WANG X., JIAO H. and LIN H. (2011) Dexamethasone-induced hepatic lipogenesis is insulin dependent in chickens. Stress-the International Journal on the Biology of Stress 14: 273-281.
CHALLENGER W.O., WILLIAMS T.D., CHRISTIANS J.K. and VEZINA F. (2001) Follicular development and plasma yolk precursor dynamics through the laying cycle in the European starling (Sturnus vulgaris). Physiological and Biochemical Zoology 74: 356-365.
COVASA M. and FORBES J.M. (1995) Selection of foods by broiler chickens following corticosterone administration. British Poultry Science 36: 489-501.
DAWSON A., KING V.M., BENTLEY G.E. and BALL G.F. (2001) Photoperiodic control of seasonality in birds. Journal of Biological Rhythms 16: 365-380.
DECUYPERE E. and VERHEYEN G. (1986) Physiological basis of induced moulting and tissue regeneration in fowls. World's Poultry Science Journal 42: 56-68.
DHILLON S.S., GINGERICH S. and BELSHAM D.D. (2009) Neuropeptide Y induces gonadotropin-releasing hormone gene expression directly and through conditioned medium from mHypoE-38 NPY neurons. Regulatory Peptides 156: 96-103.
DOBSON H., ESSAWY S.A. and ALAM M.G. (1988) Suppression of LH response to gonadotrophin-releasing hormone or oestradiol by ACTH(1-24) treatment in anoestrous ewes. Journal of Endocrinology 118: 193-197.
DUBEY A.K. and PLANT T.M. (1985) A suppression of gonadotropin secretion by cortisol in castrated male rhesus monkeys (Macaca mulatta) mediated by the interruption of hypothalamic gonadotropin-releasing hormone release. Biology of Reproduction 33: 423-431.
DUNN I.C., MIAO Y.W., MORRIS A., ROMANOV M.N., WILSON P.W. and WADDINGTON D. (2004) A study of association between genetic markers in candidate genes and reproductive traits in one generation of a commercial broiler breeder hen population. Heredity 92: 128-134.
EL-LETHEY H., JUNGI T.W. and HUBER-EICHER B. (2001) Effects of feeding corticosterone and housing conditions on feather pecking in laying hens (Gallus gallus domesticus). Physiology & Behavior 73: 243-251.
ETCHES R.J., WILLIAMS J.B. and RZASA J. (1984) Effects of corticosterone and dietary changes in the hen on ovarian function, plasma LH and steroids and the response to exogenous LH-RH. Journal of Reproduction and Fertility 70: 121-130.
EUKER J.S., MEITES J. and RIEGLE G.D. (1975) Effects of acute stress on serum LH and prolactin in intact, castrate and dexamethasone-treated male rats. Endocrinology 96: 85-92.
EVANS J.J. and ANDERSON G.M. (2012) Balancing ovulation and anovulation: integration of the reproductive and energy balance axes by neuropeptides. Human Reproduction Update 18: 313-332.
FURUSE M., HATA M., FURUSE K., YOSHIDA Y., HARATAKE A., SUGITANI Y., NODA T., KUBO A. and TSUKITA S. (2002) Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson from claudin-1-deficient mice. Journal of Cell Biology 156: 1099-1111.
GAMBACCIANI M., YEN S. and RASMUSSEN D. (1986) GnRH release from the mediobasal hypothalamus: in vitro inhibition by CRF. Neuroendocrinology 43: 533-536.
GARLICH J., BRAKE J., PARKHURST C.R., THAXTON J.P. and MORGAN G.W. (1984) Physiological profile of caged layers during one production year, molt, and postmolt: egg production, egg shell quality, liver, femur, and blood parameters. Poultry Science 63: 339-343.
GERIS K.L., BERGHMAN L.R., KUHN E.R. and DARRAS V.M. (1999) The drop in plasma thyrotropin concentrations in fasted chickens is caused by an action at the level of the hypothalamus: role of corticosterone. Domestic Animal Endocrinology 16: 231-237.
GONZALES C., VOIROL M.J., GIACOMINI M., GAILLARD R.C., PEDRAZZINI T. and PRALONG F.P. (2004) The neuropeptide Y Y1 receptor mediates NPY-induced inhibition of the gonadotrope axis under poor metabolic conditions. FASEB Journal 18: 137-139.
GOUTTE A., CLEMENT-CHASTEL C., MOE B., BECH C., GABRIELSEN G.W. and CHASTEL O. (2011) Experimentally reduced corticosterone release promotes early breeding in black-legged kittiwakes. Journal of Experimental Biology 214: 2005-2013.
HAYASHI K. and MOBERG G. (1990) Influence of the HPA axis on the menstrual cycle and the pituitary responsiveness to estradiol in the female rhesus monkey. Biology of Reproduction 42: 260-265.
HENRIKSEN R., GROOTHUIS T.G. and RETTENBACHER S. (2011) Elevated plasma corticosterone decreases yolk testosterone and progesterone in chickens: linking maternal stress and hormone-mediated maternal effects. Plos One 6: e23824.
HILAL E.M., CHEN J.H. and SILVERMAN A.J. (1996) Joint migration of gonadotropin-releasing hormone (GnRH) and neuropeptide Y (NPY) neurons from olfactory placode to central nervous system. Journal of Neurobiology 31: 487-502.
HOLMES W.N. and PHILLIPS J.G. (1976) The adrenal cortex of birds, in: CHESTER-JONES, I. & HENDERSON, I. (Eds) General, Comparative and Clinical Endocrinology of the Adrenal Cortex, pp. 293-420 (New York, Academic Press).
JENNI-EIERMANN S., GLAUS E., GRUEBLER M., SCHWABL H. and JENNI L. (2008) . Glucocorticoid response to food availability in breeding barn swallows (Hirundo rustica). General & Comparative Endocrinology 155: 558-565.
KAHN B.B., ALQUIER T., CARLING D. and HARDIE D.G. (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metabolism 1: 15-25.
KALRA S.P. and KALRA P.S. (2004) NPY: a novel on/off switch for control of appetite and reproduction, in: MICHEL, M.C. (Ed.) Neuropeptide Y and related peptides, pp. 221-249 (Berlin, Springer-Verlag).
KALRA S.P., CLARK J.T., SAHU A., DUBE M.G. and KALRA P.S. (1988) Control of feeding and sexual behaviors by neuropeptide Y: physiological implications. Synapse 2: 254-257.
KALRA S.P., XU B., DUBE M.G., MOLDAWER L.L., MARTIN D. and KALRA P.S. (1998) Leptin and ciliary neurotropic factor (CNTF) inhibit fasting-induced suppression of luteinizing hormone release in rats: role of neuropeptide Y. Neuroscience Letters 240: 45-49.
KIM M.S., PARK J.Y., NAMKOONG C., JANG P.G., RYU J.W., SONG H.S., YUN J.Y., NAMGOONG I.S., HA J., PARK I.S., LEE I.K., VIOLLET B., YOUN J.H., LEE H.K. and LEE K.U. (2004) Anti-obesity effects of α-lipoic acid mediated by suppression of hypothalamic AMP-activated protein kinase. Nature Medicine 10: 727-733.
KIM J. and CHOI Y.H. (2014) Differential abundance of egg white proteins in laying hens treated with corticosterone. Journal of Agricultural and Food Chemistry 62: 12346-12359.
KIRCHGESSNER T.G., HEINZMANN C., SVENSON K.L., GORDON D.A., NICOSIA M., LEBHERZ H.G., LUSIS A.J. and WILLIAMS D.L. (1987) Regulation of chicken apolipoprotein B: cloning, tissue distribution, and estrogen induction of mRNA. Gene 59: 241-251.
KLENKE U., CONSTANTIN S. and WRAY S. (2010) Neuropeptide Y directly inhibits neuronal activity in a subpopulation of gonadotropin-releasing hormone-1 neurons via Y1 receptors. Endocrinology 151: 2736-2746.
KUENZEL W.J. (2000) Central nervous system regulation of gonadal development in the avian male. Poultry Science 79: 1679-1688.
KUKSIS A. (1992) Yolk Lipids. Biochimica et Biophysica Acta 1124: 205-222.
LENNARTSSON A.K., KUSHNIR M.M., BERGQUIST J., BILLIG H. and JONSDOTTIR I.H. (2012) Sex steroid levels temporarily increase in response to acute psychosocial stress in healthy men and women. International Journal of Psychophysiology 84: 246-253.
LI H.F., ZHU W.Q., CHEN K.W., WU X., TANG Q.P., GAO Y.S., SONG W.T. and XU H.L. (2009) Polymorphism in NPY and IGF-I genes associate with reproductive traits in Wenchang chicken. African Journal of Biotechnology 8: 4744-4748.
LIN H., DECUYPERE E. and BUYSE J. (2004) Oxidative stress induced by corticosterone administration in broiler chickens (Gallus gallus domesticus) 2. short-term effect. Comparative Biochemistry & Physiology Part B Biochemistry & Molecular Biology 139: 745-751.
LIU L., SONG Z.G., KONG X., JIAO H.C. and LIN H. (2012a) Effects of dexamethasone and dietary energy level on energy intake and neuropeptide Y gene expression of broiler chickens. Chinese Journal of Animal Nutrition 24: 95-103.
LIU L., SONG Z.G., SHEIKHAHMADI A., JIAO H.C. and LIN H. (2012b) Effect of corticosterone on gene expression of feed intake regulatory peptides in laying hens. Comparative Biochemistry & Physiology Part B Biochemistry & Molecular Biology 162: 81-87.
LIU L., LI H.P., LI X.L., JIAO H.C., LIN H., SHEIKHAHMADI A., WANG Y.F. and SONG Z.G. (2013) Effects of acute heat stress on gene expression of brain-gut neuropeptides in broiler chickens. Journal of Animal Science 91: 5194-5201.
LIU L., SONG Z.G., JIAO H.C. and LIN H. (2014) Glucocorticoids increase NPY gene expression via hypothalamic AMPK signaling in broiler chicks. Endocrinology 155: 2190-2198.
LIU L., WANG X.J., JIAO H.C., ZHAO J.P. and LIN H. (2015) Glucocorticoids inhibited hypothalamic target of rapamycin in high fat diet-fed chicks. Poultry Science 94: 2221-2227.
LYNN S.E., BREUNER C.W. and WINGFIELD J.C. (2003) Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Hormones & Behavior 43: 150-157.
MANN D.R., EVANS D.C., JACOBS V.L. and COLLINS D.C. (1986) Influence of acute intracerebroventricular (i.c.v.) administration of adrenocorticotrophin (ACTH) on LH secretion in male rats: effect of pretreatment (i.c.v.) with ACTH antiserum on the serum LH response to an acute ether stress. Journal of Endocrinology 108: 275-280.
MARIN-BIVENS C.L., KALRA S.P. and OLSTER D.H. (1998) Intraventricular injection of neuropeptide Y antisera curbs weight gain and feeding, and increases the display of sexual behaviors in obese Zucker female rats. Regulatory Peptides 75-76: 327-334.
MENG X.T., HOU N.N., WANG X.J., JIAO H.C., ZHAO J.P., SONG Z.G. and LIN H. (2013) Increased hepatic yolk precursor synthesis, secretion and facilitated uptake by follicles are involved in the rejuvenation of reproductive performance of molted hens (Gallus gallus domesticus). General & Comparative Endocrinology 194: 198-207.
MINOKOSHI Y., ALQUIER T., FURUKAWA N., KIM Y.B., LEE A., XUE B., MU J., FOUFELLE F., FERRE P., BIRNBAUM M.J., STUCK B.J. and KAHN B.B. (2004) AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428: 569-574.
NIMPF J. and SCHNEIDER W.J. (1991) Receptor-mediated lipoprotein transport in laying hens. Journal of Nutrition 121: 1471-1474.
OAKLEY A.E., BREEN K.M., CLARKE I.J., KARSCH F.J., WAGENMAKER E.R. and TILBROOK A.J. (2009) Cortisol reduces gonadotropin-releasing hormone pulse frequency in follicular phase ewes: influence of ovarian steroids. Endocrinology 150: 341-349.
PERFITO N., ZANN R.A., BENTLEY G.E. and HAU M. (2007) Opportunism at work: habitat predictability affects reproductive readiness in free-living zebra finches. Functional Ecology 21: 291-301.
PETRAGLIA F., SUTTON S., VALE W. and PLOTSKY P. (1987) Corticotropin-releasing factor decreases plasma luteinizing hormone levels in female rats by inhibiting gonadotropin-releasing hormone release into hypophyseal-portal circulation. Endocrinology 120: 1083-1088.
PILO B., ETCHES R.J. and GEORGE J.C. (1985) Effects of corticosterone infusion on the lipogenic activity and ultrastructure of the liver of laying hens. Cytobios 44: 273-285.
POHLE K. and CHENG H.W. (2009) Comparative effects of furnished and battery cages on egg production and physiological parameters in White Leghorn hens. Poultry Science 88: 2042-2051.
PROSZKOWIEC M. and RZASA J. (2001) Variation in the ovarian and plasma progesterone and estradiol levels of the domestic hen during a pause in laying. Folia Biologica 49: 285-289.
RICHARDS M.P. (2003) Genetic regulation of feed intake and energy balance in poultry. Poultry Science 82: 907-916.
RICHARDS M.P. and PROSZKOWIEC-WEGLARZ M. (2007) Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poultry Science 86: 1478-1490.
RICHARDS M.P., ROSEBROUGH R.W., COON C.N. and MCMURTRY J.P. (2010) Feed intake regulation for the female broiler breeder: in theory and in practice. Journal of Applied Poultry Research 19: 182-193.
RORIES C., LAU C.K., FINK K. and SPELSBERG T.C. (1989) Rapid inhibition of c-myc gene expression by a glucocorticoid in the avian oviduct. Molecular Endocrinology 3: 991-1001.
ROZENBOIM I., TAKO E., GAL-GARBER O., PROUDMAN J.A. and UNI Z. (2007) The effect of heat stress on ovarian function of laying hens. Poultry Science 86: 1760-1765.
SAKETOS M., SHARMA N. and SANTORO N.F. (1993) Suppression of the hypothalamic_pituitary_ovarian axis in normal women by glucocorticoids. Biology of Reproduction 49: 1270-1276.
SCANES C.G., MERRILL G.F., FORD R., MAUSER P. and HOROWITZ C. (1980) Effects of stress (hypoglycaemia, endotoxin, and ether) on the peripheral circulating concentration of corticosterone in the domestic fowl (Gallus domesticus). Comparative Biochemistry & Physiology Part C Comparative Pharmacology 66: 183-186.
SCANES C.G., SHARP P.J., HARVEY S., GODDEN P.M.M., CHADWICK A. and NEWCOMER W.S. (1979) Variations in plasma prolactin, thyroid hormones, gonadal steroids, and growth hormone in turkeys during the induction of egg laying and molt by different photoperiods. British Poultry Science 20: 143-148.
SCHNEIDER J.E. and WATTS A.G. (2002) Energy balance, ingestive behavior and reproductive success, in: PFAFF, D., ETGEN,A., FAHRBACH, S.E. & RUBIN, R.T. (Eds) Hormones, brain and behavior, pp. 435-523 (CA, Elsevier).
SCHNEIDER J.E. (2004) Energy balance and reproduction. Physiology & Behavior 81: 289-317.
SCHNEIDER W.J. (2009) Receptor-mediated mechanisms in ovarian follicle and oocyte development. General & Comparative Endocrinology 163: 18-23.
SCHUSTER M.K., SCHMIERER B., SHKUMATAVA A. and KUCHLER K. (2004) Activin A and follicle-stimulating hormone control tight junctions in avian granulosa cells by regulating occludin expression. Biology of Reproduction 70: 1493-1499.
SHERRY D.F., MROSOVSKY N. and HOGAN J.A. (1980) Weight loss and anorexia during incubation in birds. Journal of Comparative & Physiological Psychology 94: 89-98.
SHINI S. (2003) Physiologic responses of laying hens to the alternative housing systems. International Journal of Poultry Science 2: 357-360.
SHINI S., SHINI A. and HUFF G.R. (2009) Effects of chronic and repeated corticosterone administration in rearing chickens on physiology, the onset of lay and egg production of hens. Physiology & Behavior 98: 73-77.
SON Y.L., UBUKA T., NARIHIRO M., FUKUDA Y., HASUNUMA I., YAMAMOTO K., BELSHAM D.D. and TSUTSUI K. (2014) Molecular basis for the activation of gonadotropin-inhibitory hormone gene transcription by corticosterone. Endocrinology 155: 1817-1826.
SONG Z., LIU L., SHEIKHAHMADI A., JIAO H. and LIN H. (2012a) Effect of heat exposure on gene expression of feed intake regulatory peptides in laying hens. Journal of Biomedicine and Biotechnology 2012: Article ID 484869, 8 pages, doi:10.1155/2012/484869.
SONG Z.G., LIU L., YUE Y., JIAO H.C., LIN H., SHEIKHAHMADI A., EVERAERT N., DECUYPERE E. and BUYSE J. (2012b) Fasting alters protein expression of AMP-activated protein kinase in the hypothalamus of broiler chicks (Gallus gallus domesticus). General & Comparative Endocrinology 178: 546-555.
STEARNS S.C. (1992) The evolution of life histories. (Oxford, Oxford University Press).
SUNDARESAN N.R., ANISH D., SASTRY K.V., SAXENA V.K., MOHAN J. and SAXENA M. (2007) Differential expression of lipopolysaccharide-induced TNF-alpha factor (LITAF) in reproductive tissues during induced molting of white leghorn hens. Animal Reproduction Science 102: 335-342.
TANABE Y., OGAWA T. and NAKAMURA T. (1981) The effect of short-term starvation on pituitary and plasma LH, plasma estradiol and progesterone, and on pituitary response to LH-RH in the laying hen (Gallus domesticus). General & Comparative Endocrinology 43: 392-398.
TOUFEXIS D.J., KYRIAZIS D. and WOODSIDE B. (2002) Chronic neuropeptide Y Y5 receptor stimulation suppresses reproduction in virgin female and lactating rats. Journal of Neuroendocrinology 14: 492-497.
TSUTSUI K., SAIGOH E., UKENA K., TERANISHI H., FUJISAWA Y., KIKUCHI M., ISHII S. and SHARP P.J. (2000) A novel avian hypothalamic peptide inhibiting gonadotropin release Biochem. Biochemical and Biophysical Research Communications 275: 661-667.
TURNER A.I, HEMSWORTH P.H., CANNY B.J. and TILBROOK A.J. (1999a) Inhibition of the secretion of LH in ovariectomised pigs by sustained but not repeated acute elevation of cortisol in the absence but not the presence of oestradiol. Journal of Endocrinology 163: 477-486.
TURNER A.I, HEMSWORTH P.H., CANNY B.J. and TILBROOK A.J. (1999b) Sustained but not repeated acute elevation of cortisol impaired the luteinizing hormone surge, estrus, and ovulation in gilts. Biology of Reproduction 61: 614-620.
TURPEN C., JOHNSON D.C. and DUNN J.D. (1976) Stress-induced gonadotropin and prolactin secretory patterns. Neuroendocrinology 20: 339-351.
VERHEYEN G., DECUYPERE E., KUHN E.R., FONTAINE G. and DE GROOTE G. (1983) Arret de la ponte par induction chez la poult. Effet de differentes methodes sur certains parameters de production et sur les concentrations en hormones thyroidiennes, en prolactine, en Ca, P, Na et en proteins dans le serum sanquine. Revue de I’ Agriculture 36: 1535-1559.
WADE G.N. and SCHNEIDER J.E. (1992) Metabolic fuels and reproduction in female mammals. Neuroscience & Biobehavioral Reviews 16: 235-272.
WADE G.N., SCHNEIDER J.E. and LI H.Y. (1996) Control of fertility by metabolic cues. American Journal of Physiology 270: 1-19.
WANG X., DAY J.R. and VASILATOS-YOUNKEN R. (2001) The distribution of neuropeptide Y gene expression in the chicken brain. Molecular and Cellular Endocrinology 174: 129-136.
WANG X.J., LIN H., SONG Z.G. and JIAO H.C. (2010) Dexamethasone facilitates lipid accumulation and mild feed restriction improves fatty acids oxidation in skeletal muscle of broiler chicks (Gallus gallus domesticus). Comparative Biochemistry & Physiology Part C Toxicology & Pharmacology 151: 447-454.
WANG X.J., LI Y., SONG Q.Q., GUO Y.Y., JIAO H.C., SONG Z.G. and LIN H. (2013) Corticosterone regulation of ovarian follicular development is dependent on the energy status of laying hens. Journal of Lipid Research 54: 1860-1876.
WELSH T.H. (Jr), BAMBINO T.H. and HSUEH A.J. (1982) Mechanism of glucocorticoid-induced suppression of testicular androgen biosynthesis in vitro. Biology of Reproduction 27: 1138-1146.
WHIRLEDGE S. and CIDLOWSKI J.A. (2010) Glucocorticoids, stress, and fertility. Minerva Endocrinologica 35: 109-125.
WILLIAMS J.B., ETCHES R.J. and RZASA J. (1985) Induction of a pause in laying by corticosterone infusion or dietary alterations: effects on the reproductive system, food consumption and body weight. British Poultry Science 26: 25-34.
WILSON S.C. and and LACASSAGNE L. (1978) The effects of dexamethasone on plasma luteinizing hormone and oviposition in the hen (Gallus domesticus). General and Comparative Endocrinology 35: 16-26.
WINGFIELD J.C. (1985) Influences of weather on reproductive function in female Song sparrows, Melospiza melodia. Journal of Zoology 205: 525-544.
WÓJCIK-GLADYSZ A. and POLKOWSKA J. (2006) Neuropeptide Y-a neuromodulatory link between nutrition and reproduction at the central nervous system level. Reproductive Biology 6: 21-28.
WU X., LI H., YAN M., TANG Q., CHEN K., WANG J., GAO Y., TU Y., YU Y. and ZHU W. (2007) Associations of Gonadotropin-Releasing Hormone Receptor (GnRHR) and Neuropeptide Y (NPY) Genes' Polymorphisms with Egg-Laying Traits in Wenchang Chicken. Agricultural Sciences in China 6: 499-504.
YEN C.F., JIANG Y.N., SHEN T.F., WONG I.M., CHEN C.C., CHEN K.C., CHANG W.C., TSAO Y.K. and DING S.T. (2005) Cloning and expression of the genes associated with lipid metabolism in Tsaiya ducks. Poultry Science 84: 67-74.
YUAN L., LIN H., JIANG K.J., JIAO H.C. and SONG Z.G. (2008) Corticosterone administration and high-energy feed results in enhanced fat accumulation and insulin resistance in broiler chickens. British Poultry Science 49: 487-495.
ZHAO J.P., ZHANG Q., JIAO H.C., WANG X.J., JIANG M.J., LUO H. and LIN H. (2016) Ovalbumin expression in the oviduct magnum of hens is related to the rate of egg laying and shows distinct stress-type-specific responses. Journal of Animal Physiology and Animal Nutrition 100: 876-883.
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