Maternal corticosterone reduces egg fertility and hatchability and increases the numbers of early dead embryos in eggs laid by quail hens selected for exaggerated adrenocortical stress responsiveness (original) (raw)

Influence of maternal corticosterone treatment on incubation length of eggs laid by Japanese quail hens selected for divergent adrenocortical stress responsiveness

British Poultry Science, 2009

1. Previous studies have shown that more yolk corticosterone is found in the eggs of random bred Japanese quail hens implanted with corticosterone during egg formation; both unstressed and stressed quail hens selected for exaggerated (high stress) rather than reduced (low stress) plasma corticosterone response to brief restraint deposit more corticosterone into their egg yolks. The length of egg incubation is also known to be shorter in eggs laid by high than low stress hens. 2. Here we investigated the interactive effects of quail stress line (low vs. high stress) with maternal corticosterone treatment (empty implant controls vs. corticosterone-implants) during egg formation on length of egg incubation. 3. Mean (AESEM) length of egg incubation for high stress control eggs (397Á3 AE 0Á4 h) was similarly shorter (by about 4.5 h) than that found for low stress control eggs (392Á8 AE 0Á2 h). In addition, on average, the incubation length of eggs laid by corticosterone-implanted hens (392Á9 AE 0Á5 h) was nearly 3 h shorter than that found for eggs laid by control hens (395Á8 AE 0Á2 h) regardless of stress line. 4. Line  hen-implant treatment effects on mean (AESEM) length of egg incubation partitioned in rank order as follows: low stress control (397Á8 AE 0Á5 h)4low stress corticosterone-implant (395Á9 AE 0Á7 h)4high stress control (393Á8 AE 0Á3 h)4high stress corticosterone-implant (391Á2 AE 0Á4 h). 5. Our original contention that selection for exaggerated adrenocortical responsiveness is associated with a reduction in the length of egg incubation was supported. Because maternal stress-induced elevations of yolk B are known to occur, the present findings of further shortenings of the hatching times of eggs of corticosterone-treated hens of both stress lines are also important to the poultry industry because they warn producers that unless stress in hens during egg formation is minimised, abbreviated egg incubation periods may result beyond the effects that a hen's genetic predisposition to adrenocortical stress responsiveness has on the length of egg incubation.

REPRODUCTIVE FUNCTION IN HYBRID POULTRY. IV. AN IMPACT OF MATERNAL HORMONES ACCUMULATED IN EGG

Deposit of maternal hormones in the egg yolk is shown to significantly change the pattern of ontogenesis in descendants. Accumulation of maternal sexual steroids in yolk influences behavior, growth, morphology, immune function and viability of descendants (T. Groothuis et al., 2005). Testosterone and androstenedione cause changes in postnatal growth (H. Schwabl, 1996), immunocompetence (M.Tobler et al., 2010), models of competitive and agonistic behavior in non-reproductive relationships between individuals (Müller W. et al., 2009) and sexual intercourse (C .Eising et al., 2006). Such consequences develop as a result of regulation of corresponding functions in the descendant body, including indirect influence through other systems. Stress simulation in females by administration of corticosterone (K) led to a dose dependent change in growth and development in the chicken. Imbalance in fatty acids’ ratio and assimilation in descendant embryo occurred in the yolk (S. Yalçın et al., 2011) reduce fertility and shell quality, and embryo mortality and death of chicks increase (M. Eriksen et al., 2003; Saino N. et al., 2005; Y.-H. Kim et al., 2014). Similar effects were found in the offspring of hens lines divergently selected by growth rate (A. Abdelkareem et al., 2013). In the yolk of white shell eggs of unstressed layers the corticosterone level is almost two times higher than that in brown shell eggs (K. Navara et al., 2010). Under the influence of different stress factors the activity of the hypothalamic-pituitary-gonadal axis alters, resulting in an inadequate kinetics of sex hormones and inhibition of the reproductive function. Increased concentration of blood corticosterone in the mother hens is accompanied by changes in the content of gonadal hormones in the egg yolk (A. Janczak et al., 2009; F. Guibert et al., 2013), productivity (A. Bertin et al., 2008; E. de Haas et al., 2013) and the sex ratio (S. Correa et al., 2005; T. Pike et al., 2005; S. Pryke et al., 2011). Migration of the hormones form a mother hen to the egg and the embryo, and their interference in metabolism regulation in the descendant occur during early ontogenesis, when the functions of organs and systems are the most labile. Changes in ontogenesis caused by accumulated maternal hormones can be regarded as an adaptive response in the descendants to be ready to a shift in environmental conditions (T. Mousseau et al., 1998; Z. Kankova et al., 2012). Due to egg-deposited maternal hormones the offspring can form phenotypic traits which are inherited epigenetically (T. Groothuis et al., 2008; D. Ho et al., 2011). All these finding should be taken into account at poultry commercial reproduction. When using technological methods and veterinary measures, it is necessary to appreciate possibility of transovarial transfer of signal information about outer conditions mediated by the maternal hormones to cause adaptations in the descendants. Keywords: bird, egg, maternal hormones, accumulation, stress, ontogenesis descendants

Maternal corticosterone elevation during egg formation in chickens (Gallus gallus domesticus) influences offspring traits, partly via prenatal undernutrition

General and Comparative Endocrinology, 2013

The relationship between maternal stress during pregnancy in humans and the subsequent physical and mental health disorders in their children has inspired a wide array of studies on animal models. Almost all of these studies have used mammalian species, but more recently oviparous species in which the embryo develops outside the mother's body have received more attention. These new models facilitate disentangling of the underlying mechanism due to the accessibility of the prenatal environment, the egg. Studies in birds have found that maternal stress during egg formation induces phenotypic alterations in the offspring that hatch from these eggs. However, different offspring traits have been measured in different studies and potential underlying mechanisms are barely addressed. In this study we experimentally manipulated maternal corticosterone levels in laying hens. We found that mothers with experimentally elevated plasma corticosterone levels produced offspring that are smaller at hatching, less competitive, less fearful, have lower immunocompetence and higher plasma testosterone levels, as well as an alteration of visually guided behavioural lateralization. Earlier we have showed that eggs produced by these corticosterone treated mothers were lighter and contained lower concentrations of testosterone and progesterone in the yolk. While yolk hormones showed no correlation with any offspring traits, egg mass correlated positively with offspring's body mass from hatching until 10 days of age and hatching mass correlated positively with the offspring's ability to compete for food, indicating that prenatal under nutrition might mediate some effects of maternal stress.

Elevated Plasma Corticosterone Decreases Yolk Testosterone and Progesterone in Chickens: Linking Maternal Stress and Hormone-Mediated Maternal Effects

PLoS ONE, 2011

Despite considerable research on hormone-mediated maternal effects in birds, the underlying physiology remains poorly understood. This study investigated a potential regulation mechanism for differential accumulation of gonadal hormones in bird eggs. Across vertebrates, glucocorticoids can suppress reproduction by downregulating gonadal hormones. Using the chicken as a model species, we therefore tested whether elevated levels of plasma corticosterone in female birds influence the production of gonadal steroids by the ovarian follicles and thus the amount of reproductive hormones in the egg yolk. Adult laying hens of two different strains (ISA brown and white Leghorn) were implanted subcutaneously with corticosterone pellets that elevated plasma corticosterone concentrations over a period of nine days. Steroid hormones were subsequently quantified in plasma and yolk. Corticosterone-implanted hens of both strains had lower plasma progesterone and testosterone levels and their yolks contained less progesterone and testosterone. The treatment also reduced egg and yolk mass. Plasma estrogen concentrations decreased in white Leghorns only whereas in both strains yolk estrogens were unaffected. Our results demonstrate for the first time that maternal plasma corticosterone levels influence reproductive hormone concentrations in the yolk. Maternal corticosterone could therefore mediate environmentally induced changes in yolk gonadal hormone concentrations. In addition, stressful situations experienced by the bird mother might affect the offspring via reduced amounts of reproductive hormones present in the egg as well as available nutrients for the embryo.

Effects of chronic and repeated corticosterone administration in rearing chickens on physiology, the onset of lay and egg production of hens

Physiology & Behavior, 2009

A corticosterone model was used to study the effects of chronic and repeated stress during the rearing phase on physiology, the onset of lay and performance of laying hens in the subsequent laying period. Two hundred and seventy Hy-line brown layer pullets were reared in environmentally controlled battery cages. At 7, 11, and 15 weeks of age birds were exposed for 1 week to the following treatments in drinking water: corticosterone dissolved in ethanol, ethanol, or untreated water. One week following each treatment, and at 35 weeks of age endocrine, metabolic and haematological tests were conducted. Body weight was measured throughout the study, and egg production was recorded daily throughout the laying period. Plasma corticosterone levels and heterophil to lymphocyte (H/L) ratio were increased after each corticosterone delivery, showing the effectiveness of the treatment. When corticosterone delivery was interrupted, plasma corticosterone and H/L ratio were significantly reduced. Exposing birds to repeated and long-term corticosterone treatment significantly affected BW (P b 0.01), and relative organ weights (P b 0.01). Corticosterone delivery also resulted in increased blood levels of glucose (GLU), cholesterol (CHOL), and triglyceride (TRG). Administration of corticosterone during the rearing phase delayed the onset of lay and decreased egg production at 35 weeks of age. These results demonstrate that oral corticosterone treatment affects hen physiology, reduces performance, and may model the effects of production stressors.

The relationship between pre-laying activity and corticosterone concentrations, and the interpretation for laying hen welfare

Some opponents of cage housing for laying hens argue that nest boxes are important for hen welfare. Evidence to support this argument is that most hens choose to lay in a nest box if available (i.e. hens show preference), and hens are more active in the absence of a nest box and may perform pacing before egg laying (i.e. hens show frustration). In this experiment, in which hens were housed in groups of 2, 4 or 8 in 8-bird cages with and without a nest box, we investigated the relationship between pre-laying activity and basal stress levels, measured via corticosterone in eggs and plasma (~4-5 h post-laying). The posture and behaviour of 58 Hy-line Brown hens during 2-h pre-laying were collated from video records for a total of 135 egg-laying events. Hens that displayed more bouts of sitting posture, or that spent less time sitting, had higher plasma corticosterone concentrations. Further, hens that displayed more pre-laying activity had lower plasma corticosterone concentrations, although the occurrence of walk/run behaviour was not associated with plasma corticosterone. Lower activity, increased frequency of sitting and reduced time spent sitting prior to oviposition may reflect increased stress as indicated by the higher plasma corticosterone concentrations. While the evidence is limited, the finding that some pre-laying activities of hens were related to plasma corticosterone concentrations is contrary to expectation, and highlights a lack understanding of the relevance of pre-laying activity and sitting posture to layer hen welfare.

Neonatal stimulation improves egg production in laying hens

2011

Fil: Cid, Mariana Paula. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - Cordoba. Instituto de Investigaciones Biologicas y Tecnologicas. Universidad Nacional de Cordoba. Facultad de Ciencias Exactas, Fisicas y Naturales. Instituto de Investigaciones Biologicas y Tecnologicas; Argentina. Universidad Nacional de Cordoba. Facultad de Ciencias Quimicas. Departamento de Quimica Biologica; Argentina

Novel insights into relationships between egg corticosterone and timing of breeding revealed by LC-MS/MS

Journal of Avian Biology, 2015

Inter-and intra-clutch variation in egg corticosterone (CORT), the major glucocorticoid in birds, may provide insights into how maternal stress levels vary with the timing of breeding and with laying order. Common analytical methods (e.g. immunoassays), however, suffer from cross-reaction with other steroids, leading to potential overestimation of CORT concentrations which can obscure true hormone-environment relationships and complicate among-study comparisons. We here apply a new LC-MS/MS technique, which has recently been shown to avoid the problem of cross-reactivity due to its high specificity, to quantify CORT concentrations in yolk and albumen in clutches of lesser black-backed gulls Larus fuscus. We found that CORT concentration exhibited a previously unreported U-shaped relationship with time of breeding, which we explain as a potential interplay of two forces exerting extra strain on the early and late breeders. Furthermore, results showed an increase in CORT with laying order indicating the energetic expense of egg production. The levels of CORT assessed in this study were significantly lower than those previously reported in studies using immunoassays for CORT analysis. This supports the fact that incorporating chromatography effectively reduces overestimation of CORT due to cross-reactivity with other steroid hormones, particularly in egg yolk.

Effect of maternal environment on yolk immunoreactive corticosterone and its influence on adrenocortical and behavioral activity in chicks of Greater Rhea (Rhea americana

Hormones and Behavior, 2019

Maternal corticosterone in avian eggs may modify offspring phenotype in order to increase survival in poor environments. In the Greater Rhea (Rhea americana), we previously found that yolk immunoreactive corticos-terone is influenced by the quality of the maternal environment: eggs laid by females of the intensive rearing system (IRS), living in poor captive conditions, had higher yolk immunoreactive corticosterone than those produced by females of the semi-extensive rearing system (SRS), living in better conditions. Here, we evaluate if these different hormone levels are associated with the production of different phenotypes. We collected eggs from the IRS and SRS for hormonal quantification and artificial incubation. Then, half of the chicks selected from each environment were exposed to a capture and restraint protocol, and the rest remained undisturbed and were used as controls. In the IRS, we found that higher yolk immunoreactive corticosterone was associated with the production of chicks that had reduced hatchability, lower hatchling mass and higher baseline fecal glucocorti-coid metabolites (FGM) than those produced by SRS females. Moreover, after capture and restraint, IRS chicks did not modify their FGM nor their behaviors compared to their controls, while SRS chicks increased their FGM and spent more time ambulating and less time pecking, compared to their controls. These results indicate that yolk immunoreactive corticosterone could modify offspring phenotype. Although future studies are needed to elucidate their implications for fitness, our results suggest that yolk corticosterone could be mediating an adaptive maternal effect that allows individuals to better cope with poor conditions.

Invasive and noninvasive measurement of stress in laying hens kept in conventional cages and in floor pens

Poultry Science, 2009

Measurements of the heterophil:lymphocyte (H/L) ratio (invasive technique) and corticosterone in yolk and albumen (noninvasive techniques) were used to measure stress in 3 commercial laying strains, Lohmann White (LW), H&N White (HN), Lohmann Brown (LB), and a noncommercial cross (CR) between Rhode Island Red (male) and Barred Plymouth Rock (female), kept in conventional cages or floor pens. All chicks were reared in their respective environments, and 450 and 432 pullets were placed at 18 and 7 wk of age in cages and floor pens, respectively. Blood from 12 hens per strain was taken at 19, 35, and 45 wk of age in each housing system. A total of 100 heterophils and lymphocytes were counted and their ratio (H/L ratio) was calculated. Corticosterone was measured in yolk and albumen from 12 hens per strain in each housing system at 22 and 45 wk of age. The H/L ratio was within the normal range. The interaction between en-vironment and strain for the H/L ratio showed that in both environments, LB and CR hens had a higher H/L ratio than LW and HN layers. In cages, there were significant differences in H/L ratios between LW and HN hens that were likely due to genetic differences. The LW hens had significantly lower corticosterone concentrations in yolk than LB hens. In cages but not floor pens, yolk corticosterone concentrations at wk 22 were significantly higher than at wk 45. In floor pens but not cages, albumen corticosterone at wk 22 was higher than at wk 45. The H/L ratios suggest that none of the hens were unduly stressed, and corticosterone levels in yolk and albumen support the suggestion that hens adapted to their environments with age. Although measurement of yolk corticosterone and the H/L ratio may be comparable, the measurement of corticosterone level in the albumen may differ because it is secreted over a short time.