Hostname: page-component-74656f9884-8r8nv Total loading time: 0 Render date: 2026-11-06T23:16:05.711Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  19 October 2017

X.J. WANG ,
L. LIU ,
J.P. ZHAO ,
H.C. JIAO  and
H. LIN
X.J. WANG
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Department of Animal Science, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province, 271018, China
L. LIU
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Department of Animal Science, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province, 271018, China
J.P. ZHAO
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Department of Animal Science, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province, 271018, China
H.C. JIAO
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Department of Animal Science, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province, 271018, China
H. LIN*
Affiliation:
Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Department of Animal Science, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province, 271018, China
*
Corresponding author: hailin@sdau.edu.cn

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.

Keywords

stressenergyglucocorticoidsreproductionlaying hens

Information

Type
Reviews
Information
World's Poultry Science Journal , Volume 73 , Issue 4 , December 2017 , pp. 845 - 856
Copyright
Copyright © World's Poultry Science Association 2017 

Introduction

In the face of potentially stressful challenges, activations of neural, neuroendocrine and immune systems promote adaption (termed ‘allostasis’) to maintain homeostasis. However, these allostatic systems can cause maladaption or disease if they are overactive or underactive over long periods. It thus appears that the stress response has both positive and negative effects. Despite the obvious positive effects of the stress response for homeostasis and health, the negative effects for the body have recently received increasing attention.

For laying hens reared under commercial conditions, stress is a common problem disrupting their physiological homeostasis and laying performance (Shini, Reference SHINI2003; Pohle and Cheng, Reference POHLE and CHENG2009). Such birds are exposed to various stressors such as repeated restraint (i.e., weighing, vaccination, moving to the layer shed, etc.) and a variety of environmental changes. These challenges typically trigger a cascade of endocrine secretions involving the hypothalamic-pituitary-adrenal (HPA) axis, which regulates secretion of glucocorticoids to mediate the necessary allostatic adjustments (Blas, Reference BLAS2015). Corticosterone is the predominant avian glucocorticoid and a hallmark of the adrenocortical response to stress in birds (Blas, Reference BLAS2015). Glucocorticoids transmit information about environmental conditions to the hypothalamic-pituitary-gonadal (HPG) axis, which ultimately influences egg production. Energy intake and distribution between organs or tissues are influenced.

Glucocorticoids and energy intake

evoked HPA axis responses: a consequence of energy deficiencies

A stressful environment causes an energetic challenge. The critical role of glucocorticoids in the regulation of energy balance in response to the energetic challenge caused by a stressor is well documented. Plasma levels of corticosterone, the primary glucocorticoid in birds (Holmes and Phillips, Reference HOLMES and PHILLIPS1976), are increased during periods of reduced food supply associated with cold and poor weather (Wingfield, Reference WINGFIELD1985; Astheimer et al., Reference ASTHEIMER, BUTTEMER and WINGFIELD1995; Jenni-Eiermann et al., Reference JENNI-EIERMANN, GLAUS, GRUEBLER, SCHWABL and JENNI2008) and during periods of experimental acute fasting (Lynn et al., Reference LYNN, BREUNER and WINGFIELD2003). Although corticosterone responses to fasting can vary among individuals and depend on energy reserves and experience (Richards, Reference RICHARDS2003), the majority of studies demonstrated an elevated corticosterone concentration during fasting challenge in chickens. An increase in plasma corticosterone is observed after food deprivation in both immature (Geris et al., Reference GERIS, BERGHMAN, KUHN and DARRAS1999) and adult chickens (Scanes et al., Reference SCANES, MERRILL, FORD, MAUSER and HOROWITZ1980). This means that food shortage acts as a potent activator of the HPA axis in birds, supporting the suggestion that a link exists between food availability and HPA axis activation in birds (Lynn et al., Reference LYNN, BREUNER and WINGFIELD2003). Given the critical role of glucocorticoids in the regulation of energy balance, it is possible that glucocorticoid secretion in response to energy constraints such as fasting act through a series of mechanisms, thereby suppressing egg-laying when conditions are not appropriate to support breeding (Perfito et al., Reference PERFITO, ZANN, BENTLEY and HAU2007).

Glucocorticoids and appetite

A number of reports document the effect of glucocorticoids on the food intake of chickens. Corticosterone induces a dose-dependent increase in food intake in poultry (Covasa and Forbes, Reference COVASA and FORBES1995; El-Lethey et al., Reference EL-LETHEY, JUNGI and HUBER-EICHER2001; Liu et al., Reference LIU, SONG, JIAO and LIN2014) and is involved in the control of appetite (Yuan et al., Reference YUAN, LIN, JIANG, JIAO and SONG2008). Moreover, the effect of corticosterone on food intake in birds depends on their diets, that is, corticosterone-challenge, causes a high-energy diet preference, such as high-protein diets (Bartov, Reference BARTOV1985) and high-fat diets (Liu et al., Reference LIU, SONG, KONG, JIAO and LIN2012a). Several features of high-fat foods, such as palatable flavour and delayed satiating effects, may contribute to the overeating response (Blundell and MacDiarmid, Reference BLUNDELL and MACDIARMID1997).

Many neuropeptides, so-called appetite regulatory peptides, are expressed in the hypothalamus and gastrointestinal tract and are involved in the regulation of food intake in birds (Richards and Proszkowiec-Weglarz, Reference RICHARDS and PROSZKOWIEC-WEGLARZ2007). A dynamic balance between appetite-associated peptides in the hypothalamus and gastrointestinal tract controls the feeding status of chickens under glucocorticoid treatment (Liu et al., Reference LIU, SONG, SHEIKHAHMADI, JIAO and LIN2012b). Some gastrointestinal tract peptides, such as ghrelin and cholecystokinin (CCK), may play pivotal roles in the reduction of food intake in both immature chickens (Liu et al., Reference LIU, LI, LI, JIAO, LIN, SHEIKHAHMADI, WANG and SONG2013) and laying hens (Song et al., Reference SONG, LIU, SHEIKHAHMADI, JIAO and LIN2012a) exposed to heat stress, whereas some hypothalamic neurons, such as neuropeptide Y (NPY), are associated with the regulation of appetite by glucocorticoids (Liu et al., Reference LIU, SONG, JIAO and LIN2014; Reference LIU, WANG, JIAO, ZHAO and LIN2015).

The hypothalamus is important in interpreting external environmental cues such as stressors and generates the appropriate responses for food intake in birds (Richards et al., Reference RICHARDS, ROSEBROUGH, COON and MCMURTRY2010). It is well-recognised that hypothalamic AMP-activated protein kinase (AMPK) signalling is involved in the control of food intake (Minokoshi et al., Reference MINOKOSHI, ALQUIER, FURUKAWA, KIM, LEE, XUE, MU, FOUFELLE, FERRE, BIRNBAUM, STUCK and KAHN2004). AMPK acts as a sensor of cellular energy changes and is activated by increasing AMP levels coupled with decreasing ATP levels. After activation, AMPK phosphorylates acetyl-CoA carboxylase (ACC) and initiates energy-producing pathways at the expense of energy-depleting processes (Kahn et al., Reference KAHN, ALQUIER, CARLING and HARDIE2005). Fasting evokes hypothalamic AMPK activation in chicks (Song et al., Reference SONG, LIU, YUE, JIAO, LIN, SHEIKHAHMADI, EVERAERT, DECUYPERE and BUYSE2012b). Activated AMPK stimulates NPY gene expression and food intake, whereas the inactivated AMPK induces anorexia in chicks (Kim et al., Reference KIM, PARK, NAMKOONG, JANG, RYU, SONG, YUN, NAMGOONG, HA, PARK, LEE, VIOLLET, YOUN, LEE and LEE2004; Liu et al., Reference LIU, SONG, JIAO and LIN2014). Moreover, a recent study indicated that corticosterone challenge causes a high-fat diet preference by enhancing NPY expression via the AMPK pathway in the hypothalamus. Liu et al. (Reference LIU, WANG, JIAO, ZHAO and LIN2015) suggested a potential role for the target of rapamycin (TOR) pathway of hypothalamus in the regulation of appetite-related genes by glucocorticoids, which must be further verified.

involvement of NPY in regulation of reproduction

Appetite-associated neuropeptides also integrate the reproductive and energy balance axes (Evans and Anderson, Reference EVANS and ANDERSON2012). Of these neuropeptides, NPY is considered to function as a switch in the brain that turns on appetite and turns off reproduction. The reciprocal control of appetite and reproduction is inherent in the NPY molecule itself (Kalra and Kalra, Reference KALRA and KALRA2004). NPY is an important neuromodulator affecting gonadal function in mammals and birds (Hilal et al., Reference HILAL, CHEN and SILVERMAN1996). In mammals, NPY expression causes a breeding failure (Kalra et al., Reference KALRA, CLARK, SAHU, DUBE and KALRA1988) that is manifested by inhibiting reproductive function (Kalra et al., Reference KALRA, XU, DUBE, MOLDAWER, MARTIN and KALRA1998) and suppressing sexual behaviour (Marin-Bivens et al., Reference MARIN-BIVENS, KALRA and OLSTER1998) in a receptor-dependent manner (Toufexis et al., Reference TOUFEXIS, KYRIAZIS and WOODSIDE2002; Gonzales et al., Reference GONZALES, VOIROL, GIACOMINI, GAILLARD, PEDRAZZINI and PRALONG2004; Klenke et al., Reference KLENKE, CONSTANTIN and WRAY2010). In chickens, the close association of NPY and gonadotropin-releasing hormone (GnRH), perikarya and fibres in the brain suggests a functional interaction between the two peptides in regulating gonadal function (Kuenzel, Reference KUENZEL2000). NPY may affect egg production rate through its role in the control of ovulation (Dunn et al., Reference DUNN, MIAO, MORRIS, ROMANOV, WILSON and WADDINGTON2004; Wu et al., Reference WU, LI, YAN, TANG, CHEN, WANG, GAO, TU, YU and ZHU2007; Li et al., Reference LI, ZHU, CHEN, WU, TANG, GAO, SONG and XU2009) and the secretion of hormones such as GnRH (Wang et al., Reference WANG, DAY and VASILATOS-YOUNKEN2001). NPY is the basis of a neuromodulatory link between nutrition and reproduction at the central nervous system level (Wójcik-Gładysz and Polkowska, 2006; Dhillon et al., Reference DHILLON, GINGERICH and BELSHAM2009; Klenke et al., Reference KLENKE, CONSTANTIN and WRAY2010). From an evolutionary perspective, neuropeptides that stimulate eating enhance survival during energetic challenges by inhibiting the HPG axis.

Taken together, glucocorticoids stimulate chickens to ingest more energy to cope with environmental changes, and furthermore, reproductive processes are inhibited when food availability is low or when increased energy demands are not met by compensatory food intake.

Glucocorticoids and energy distribution

The physiological mechanisms that control energy balance are integrated with those that control reproduction (Wade and Schneider, Reference WADE and SCHNEIDER1992; Wade et al., Reference WADE, SCHNEIDER and LI1996; Schneider and Watts, Reference SCHNEIDER and WATTS2002). Normally, these mechanisms optimise reproductive success under fluctuating metabolic conditions. Under stressful conditions, however, individuals should favour their own survival over that of their offspring, particularly when breeding becomes too costly in terms of body maintenance (Stearns, Reference STEARNS1992). A stressful environment can disrupt the reproduction of laying hens by triggering physiological and behavioural changes that redistribute the bodies energy reserves.

cross talk between HPA and HPG axis

The onset of breeding involves activation of the HPG axis. The hypothalamic secretion of GnRH, together with a newly discovered hypothalamic neuropeptide gonadotropin-inhibitory hormone (GnIH) which acts in opposition to GnRH-I (Tsutsui et al., Reference TSUTSUI, SAIGOH, UKENA, TERANISHI, FUJISAWA, KIKUCHI, ISHII and SHARP2000), modulates the release of the pituitary gonadotropins, luteinising hormone (LH) and follicle-stimulating hormone (FSH) (Dawson et al., Reference DAWSON, KING, BENTLEY and BALL2001), which in turn activates the gonadal development and release of sex steroids, including oestradiol and testosterone, thereby mediating the adoption of breeding behaviours (Ball, Reference BALL1993). The changes to the HPG axis during stress are dependent on the type and duration of stimulus. In the initial phase of an acute stress response, the pituitary gonadotropins (Euker et al., Reference EUKER, MEITES and RIEGLE1975; Turpen et al., Reference TURPEN, JOHNSON and DUNN1976; Mann et al., Reference MANN, EVANS, JACOBS and COLLINS1986) and sex steroid levels (Lennartsson et al., Reference LENNARTSSON, KUSHNIR, BERGQUIST, BILLIG and JONSDOTTIR2012) may increase. During prolonged periods of stress, however, the HPG axis and the production of sex steroids could be inhibited for the sake of saving energy. In laying hens, stress such as heat (Rozenboim et al., Reference ROZENBOIM, TAKO, GAL-GARBER, PROUDMAN and UNI2007), moulting and immune challenges (Sundaresan et al., Reference SUNDARESAN, ANISH, SASTRY, SAXENA, MOHAN and SAXENA2007; Ariyadi et al., Reference ARIYADI, ISOBE and YOSHIMURA2012; Zhao et al., Reference ZHAO, ZHANG, JIAO, WANG, JIANG, LUO and LIN2016), dexamethasone injection (Rories et al., Reference RORIES, LAU, FINK and SPELSBERG1989) and dietary corticosterone (Kim and Choi, Reference KIM and CHOI2014) can affect reproductive performance, including egg production, egg quality, gene expression and protein abundance in the ovary and oviduct.

The HPG axis is vulnerable to the actions of hormones associated with the activation of the HPA axis. Hypothalamic and pituitary peptides such as corticotropin-releasing hormone (CRH) and adrenocorticotropic hormone (ACTH) may act primarily at the central level (Gambacciani et al., Reference GAMBACCIANI, YEN and RASMUSSEN1986; Petraglia et al., Reference PETRAGLIA, SUTTON, VALE and PLOTSKY1987; Dobson et al., Reference DOBSON, ESSAWY and ALAM1988), while glucocorticoids may act at multiple levels to suppress the HPG axis. Strong evidence from both in vivo and in vitro systems in mammals demonstrate that glucocorticoids decrease hypothalamic GnRH release (Dubey and Plant, Reference DUBEY and PLANT1985; Oakley et al., Reference OAKLEY, BREEN, CLARKE, KARSCH, WAGENMAKER and TILBROOK2009), inhibit the basal or GnRH-stimulated release of LH from the pituitary (Saketos et al., Reference SAKETOS, SHARMA and SANTORO1993; Turner et al., Reference TURNER, HEMSWORTH, CANNY and TILBROOK1999a, b), and reduce gonadal responsiveness to LH and concentrations of LH receptors (Bambino and Hsueh, Reference BAMBINO and HSUEH1981; Hayashi and Moberg, Reference HAYASHI and MOBERG1990), or act directly on the testis/ovary by reducing steroidogenesis and/or gametogenesis (Welsh et al., Reference WELSH, BAMBINO and HSUEH1982; Whirledge and Cidlowski, Reference WHIRLEDGE and CIDLOWSKI2010). Likewise, in birds, corticosterone disturbs reproduction at the hypothalamic level by modulating GnRH/GnIH release (Son et al., Reference SON, UBUKA, NARIHIRO, FUKUDA, HASUNUMA, YAMAMOTO, BELSHAM and TSUTSUI2014), at the pituitary level by inhibiting LH secretion (Wilson and Lacassagne, 1978; Etches et al., Reference ETCHES, WILLIAMS and RZASA1984), and at the gonadal level by inhibiting testosterone /oestradiol release (Henriksen et al., Reference HENRIKSEN, GROOTHUIS and RETTENBACHER2011; Wang et al., Reference WANG, LI, SONG, GUO, JIAO, SONG and LIN2013) and ovarian function (Wilson and Lacassagne, 1978; Etches et al., Reference ETCHES, WILLIAMS and RZASA1984). We can see that glucocorticoids link the HPA axis to the HPG axis, with the secretion of glucocorticoids via the HPA axis transmitting information about environmental conditions to the HPG axis and acting at multiple possible sites along the HPG axis, which ultimately influences egg production. Thus, a corticosterone model has been widely used to study the effects of chronic and repeated stress during the rearing phase on reproductive system development (Williams et al., Reference WILLIAMS, ETCHES and RZASA1985; Shini et al., Reference SHINI, SHINI and HUFF2009), the onset of lay (Shini et al., Reference SHINI, SHINI and HUFF2009; Goutte et al., Reference GOUTTE, CLEMENT-CHASTEL, MOE, BECH, GABRIELSEN and CHASTEL2011) and performance of laying hens in subsequent laying period (Williams et al., Reference WILLIAMS, ETCHES and RZASA1985; Shini et al., Reference SHINI, SHINI and HUFF2009).

energy distribution and reproduction

Glucocorticoids trigger physiological and behavioural adjustments that shift energy investment away from reproduction and redirect it towards survival. In immature chickens, glucocorticoids stimulate energy intake (Lin et al., Reference LIN, DECUYPERE and BUYSE2004) and enhance hepatic lipogenesis and fat deposition in adipose tissues, indicating the redistribution of energy stores (Cai et al., Reference CAI, SONG, ZHANG, WANG, JIAO and LIN2009; Reference CAI, SONG, WANG, JIAO and LIN2011; Wang et al., Reference WANG, LIN, SONG and JIAO2010). In laying hens, corticosterone results in the liver and abdominal fat pad weighing significantly more whereas the ovary and oviduct is significantly regressed (Pilo et al., Reference PILO, ETCHES and GEORGE1985). We can see that glucocorticoids increase energy deposition at the expense of reproductive function. The excess energy storage in liver and adipose tissue causes deficits in the pool of fuels available for the reproductive system (Schneider, Reference SCHNEIDER2004). Specifically, glucocorticoids impede the utilisation of yolk precursors.

Glucocorticoids alter the hepatic synthesis of yolk precursors. The development of ovarian follicles is accompanied by the deposition of a large amount of yolk. During a laying cycle, follicular development is matched with a supply of yolk precursors. Triglyceride (TG) is the primary component of yolk lipid (Kuksis, Reference KUKSIS1992), which is mainly synthesised in the liver and secreted in the form of yolk-targeted very-low density lipoprotein (VLDLy). An elevated circulating VLDLy concentration was coincident with rapid yolk development and matched the variation in total yolky follicle mass (Challenger et al., Reference CHALLENGER, WILLIAMS, CHRISTIANS and VEZINA2001). VLDLy has two associated apo-lipoproteins, apo-lipoprotein B and apo-lipoprotein VLDL-II. Avian apo-lipoprotein B is a component of specialised VLDL particles that are produced by the liver in response to oestrogen (Kirchgessner et al., Reference KIRCHGESSNER, HEINZMANN, SVENSON, GORDON, NICOSIA, LEBHERZ, LUSIS and WILLIAMS1987); Apo-lipoprotein VLDL-II mRNA is specifically expressed in the liver and up-regulated after laying (Yen et al., Reference YEN, JIANG, SHEN, WONG, CHEN, CHEN, CHANG, TSAO and DING2005). The suppressed follicular development of corticosterone-treated hens is associated with the reduced availability of yolk precursor (low levels of VLDLy and vitellogenin) and the decreased expression of apo-lipoprotein B and apo-lipoprotein VLDL-II in the liver (Wang et al., Reference WANG, LI, SONG, GUO, JIAO, SONG and LIN2013). However, lipogenic activity as well as TG content in the liver was increased (Pilo et al., Reference PILO, ETCHES and GEORGE1985; Cai et al., Reference CAI, SONG, ZHANG, WANG, JIAO and LIN2009, Reference CAI, SONG, WANG, JIAO and LIN2011; Wang et al., Reference WANG, LI, SONG, GUO, JIAO, SONG and LIN2013). On the one hand, decreased apo-lipoprotein synthesis and VLDLy secretion by the liver are responsible for the decreased availability of circulating yolk precursor to oocytes; On the other hand, increased lipogenic activity with decreased lipid secretion contributes to the heavy deposition of lipid in liver.

Glucocorticoids reduce the uptake of VLDLy by follicles. In laying hens, VLDLy and vitellogenin are taken up by growing oocytes via receptor-mediated endocytosis, and both macromolecules bind to the VLDL receptors which localize on the oocyte plasma membrane (Nimpf and Schneider, Reference NIMPF and SCHNEIDER1991). Moreover, the transport of yolk precursors from the circulation to oocytes consists of five components, including granulosa cells, in which occludin- and claudin-based tight junctions are crucial for barrier function (Furuse et al., Reference FURUSE, HATA, FURUSE, YOSHIDA, HARATAKE, SUGITANI, NODA, KUBO and TSUKITA2002; Schuster et al., Reference SCHUSTER, SCHMIERER, SHKUMATAVA and KUCHLER2004; Schneider, Reference SCHNEIDER2009). Wang et al. (Reference WANG, LI, SONG, GUO, JIAO, SONG and LIN2013) observed a drop in VLDL receptor content and an increase in the expression of the tight junction proteins occludin and claudin1 in hierarchical follicles, indicating that enhanced tight junctions further prevent yolk deposition into oocytes. Furthermore, exogenous glucocorticoids perturb the reproduction of laying hens in an energy dependent-manner, that is, corticosterone suppresses follicular development when hens are in an energy deficit but not when they are in an energy sufficient state (Wang et al., Reference WANG, LI, SONG, GUO, JIAO, SONG and LIN2013).

energy redistribution in moulting

Moulting is a special period that is naturally initiated at the end of the lay cycle in birds, and is implicated in a regression of the reproductive system followed by a rejuvenation of egg-laying potential. In wild avian species, the initiation of seasonal feather moult frequently coincides with the incubation of eggs and brooding of offspring, and egg brooding is accompanied by weight loss and spontaneous anorexia (Sherry et al., Reference SHERRY, MROSOVSKY and HOGAN1980), reflecting a change in the regulation of energy balance during moulting. In commercial laying hens, induced moulting has been used as a practical procedure allowing a second or third cycle of egg production. Numerous studies show that food and water withdrawal, which is used in commercial practice to induce moulting, leads to regression of the ovary and the cessation of egg laying (Tanabe et al., Reference TANABE, OGAWA and NAKAMURA1981; Etches et al., Reference ETCHES, WILLIAMS and RZASA1984; Proszkowiec and Rzasa, Reference PROSZKOWIEC and RZASA2001). The mechanism and causes of natural moulting are not identical with those of artificial moult (Decuypere and Verheyen, Reference DECUYPERE and VERHEYEN1986), for example, prolactin is implicated in the development of broodiness and the subsequent moult when this occurs naturally, but not in the commercial laying hen induced to moult by fasting (Scanes et al., Reference SCANES, SHARP, HARVEY, GODDEN, CHADWICK and NEWCOMER1979; Verheyen et al., Reference VERHEYEN, DECUYPERE, KUHN, FONTAINE and DE GROOTE1983). In any case, moulting is a process that requires an investment of substantial amounts of energy and nutrients and is usually temporally separated from reproduction, another energy-demanding process.

A general increase in reproductive performance following induced moulting is referred to as rejuvenation, which may be mediated by an increase in tissue sensitivity or efficiency (Brake and Thaxton, Reference BRAKE and THAXTON1979). Dramatic changes take place in the liver and reproductive systems before, during and after moulting. During one year of egg production, the lipid content in the liver increases with age and shows a dramatic decrease after moulting (Garlich et al., Reference GARLICH, BRAKE, PARKHURST, THAXTON and MORGAN1984), and enhanced hepatic yolk precursor synthesis and secretion contributes to increased post-moulting laying performance (Meng et al., Reference MENG, HOU, WANG, JIAO, ZHAO, SONG and LIN2013). The loss of support provided by ovarian steroids results in regression of the oviduct and moult (Etches et al., Reference ETCHES, WILLIAMS and RZASA1984; Berry, Reference BERRY2003). Moult enhances the sensitivity of sex hormones in F1 follicles and facilitates yolk-precursor uptake by follicles, ultimately resulting in rejuvenation of reproductive performance (Meng et al., Reference MENG, HOU, WANG, JIAO, ZHAO, SONG and LIN2013). Initiation of moulting and the subsequent dynamics of energy reserves and recovery of tissue function, may be viewed as a complex physiological process, involving endocrine systems, such as corticosterone, ovarian steroids and thyroid hormones, as well as tissue structure, such as liver, ovary and oviduct (Decuypere and Verheyen, Reference DECUYPERE and VERHEYEN1986; Berry, Reference BERRY2003). These physiological mechanisms force hens to survive without food during the moult period, not only relying on catabolism of fat reserves, but also accessing resources by involution of the reproductive organs which spares other fat and protein reserves (Berry, Reference BERRY2003).

Conclusions

Stress in laying hens leads to rapid changes of endocrine physiology consistent with HPA axis activation and HPG axis deactivation. Reproductive failure and overeating are consequences of disproportionate energy storage induced by elevated corticosterone in response to stress stimulus. To attain the highest performance and optimum feed efficiency, it is important to be aware of the following factors. (1) Genetic breeding. The higher production performance and feed conversion efficiency make today's chickens more susceptible to stress than ever before. The increasing intensity of rearing makes it necessary to reconsider the selection strategy of today's commercial breeding programme in the long run. It would be interesting to systematically investigate whether strain-specific differences in stress resistance are accompanied by different function of some genes. (2) Nutritional strategies. Given the published results, stress impairs the laying performance of hens in an energy-dependent manner. The nutritional strategies of modulating energy level to satisfy the birds’ special needs during stress seem to alleviate the disadvantages of stress in the short term. (3) Production system. Over 90% of eggs all over the world are currently produced from caged layers. The research and development of new environmental control system, especially in new equipment and operation, is an urgent need for this intensive production.

Acknowledgments

This work was supported by grants from the National Key Research Programme of China (2016YFD0500510), the China Agriculture Research System (CARS-41), the National Natural Science Foundation of China (31672441, 31301993, 31272467 and 31472114), the Natural Science Foundation of Shandong Province (ZR2014CP028), the Funds of Shandong ‘Double Tops’ Programme, and the Taishan Scholars Programme (201511023).

References

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.CrossRefGoogle ScholarPubMed
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.Google Scholar
BALL, G.F. (1993) The neural integration of environmental information by seasonally breeding birds. American Zoologist 33: 185-199.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
BERRY, W.D. (2003) The physiology of induced molting. Poultry Science 82: 971-980.CrossRefGoogle ScholarPubMed
BLAS, J. (2015) Stress in birds, in: SCANES, C.G. (Eds) Sturkie's Avian Physiology, 6th, pp. 769-810 (London, Academic Press).Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
COVASA, M. and FORBES, J.M. (1995) Selection of foods by broiler chickens following corticosterone administration. British Poultry Science 36: 489-501.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
DECUYPERE, E. and VERHEYEN, G. (1986) Physiological basis of induced moulting and tissue regeneration in fowls. World's Poultry Science Journal 42: 56-68.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
GAMBACCIANI, M., YEN, S. and RASMUSSEN, D. (1986) GnRH release from the mediobasal hypothalamus: in vitro inhibition by CRF. Neuroendocrinology 43: 533-536.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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).Google Scholar
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.Google Scholar
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.Google Scholar
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).Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
KUENZEL, W.J. (2000) Central nervous system regulation of gonadal development in the avian male. Poultry Science 79: 1679-1688.Google Scholar
KUKSIS, A. (1992) Yolk Lipids. Biochimica et Biophysica Acta 1124: 205-222.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
NIMPF, J. and SCHNEIDER, W.J. (1991) Receptor-mediated lipoprotein transport in laying hens. Journal of Nutrition 121: 1471-1474.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google ScholarPubMed
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.Google Scholar
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.Google Scholar
RICHARDS, M.P. (2003) Genetic regulation of feed intake and energy balance in poultry. Poultry Science 82: 907-916.Google Scholar
RICHARDS, M.P. and PROSZKOWIEC-WEGLARZ, M. (2007) Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poultry Science 86: 1478-1490.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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).Google Scholar
SCHNEIDER, J.E. (2004) Energy balance and reproduction. Physiology & Behavior 81: 289-317.Google Scholar
SCHNEIDER, W.J. (2009) Receptor-mediated mechanisms in ovarian follicle and oocyte development. General & Comparative Endocrinology 163: 18-23.Google Scholar
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.Google Scholar
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.Google Scholar
SHINI, S. (2003) Physiologic responses of laying hens to the alternative housing systems. International Journal of Poultry Science 2: 357-360.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
STEARNS, S.C. (1992) The evolution of life histories. (Oxford, Oxford University Press).Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
TURPEN, C., JOHNSON, D.C. and DUNN, J.D. (1976) Stress-induced gonadotropin and prolactin secretory patterns. Neuroendocrinology 20: 339-351.Google Scholar
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.Google Scholar
WADE, G.N. and SCHNEIDER, J.E. (1992) Metabolic fuels and reproduction in female mammals. Neuroscience & Biobehavioral Reviews 16: 235-272.Google Scholar
WADE, G.N., SCHNEIDER, J.E. and LI, H.Y. (1996) Control of fertility by metabolic cues. American Journal of Physiology 270: 1-19.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
WHIRLEDGE, S. and CIDLOWSKI, J.A. (2010) Glucocorticoids, stress, and fertility. Minerva Endocrinologica 35: 109-125.Google Scholar
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.Google Scholar
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.Google Scholar
WINGFIELD, J.C. (1985) Influences of weather on reproductive function in female Song sparrows, Melospiza melodia. Journal of Zoology 205: 525-544.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar