Access the full text.
Sign up today, get DeepDyve free for 14 days.
Effect of restricted feed intake in broiler breeder hens on their stress levels and the growth and immunology of their offspring †,‡,2 ‡ || ‡ ‡ Mandy Bowling, Rebecca Forder, Robert J. Hughes, Sarah Weaver, and Philip Ian Hynd † ‡ Poultry CRC, PO Box U242, University of New England, Armidale, NSW 2351, Australia; School of Animal and Veterinary Science, The University of Adelaide, Roseworthy Campus, Adelaide 5371, SA, Australia; and || South Australian Research and Development Institute, Roseworthy Campus, South Australia 5371, Australia ABSTRACT: The prenatal environment has been of lipopolysaccharide. Growth and immune shown to have significant effects on the lifelong responses of these birds were then recorded. Sex health of offspring in humans and other spe- ratio was affected by hen bodyweight, with a sig- cies. Such effects have not been studied exten- nificantly increased proportion of males hatched sively in avian species but could prove important, from heavy hens. Growth rate from 35 to 42 d of especially in the case of severe feed restriction age was reduced in male progeny from low bod- imposed on broiler breeder hens to prevent obe- yweight hens. Female progeny from heavy hens sity and reduce rate of lay. Feed restriction can responded to an immune challenge by reduced potentially affect not only nutrient supply to the live weight and increased heterophil: lymphocyte embryo but stress hormone levels within the hen. ratio, suggesting a more robust immune response This study investigated the impact of nutrient in these birds than in the progeny from lower bod- restriction of the breeder hen on growth rate and yweight hens. Overall, progeny from heavy hens immune responses in the progeny with the objec- had increased antibodies at day 35 to the vaccina- tive to measure the impact of feed restriction tion of IBV compared with progeny of low body- of broiler breeder hens on growth and immune weight hens, also suggesting an improved immune response of the progeny. Broiler breeder hens response in these birds. Breeder hens restricted were feed restricted from 24 wk of age and main- to the lowest feed level showed behaviors indic- tained at three bodyweights; 3.4, 3.6, and 4.0 kg ative of increased stress (object pecking) and until 43 wk of age and behavioral and physio- an increased heterophil: lymphocyte ratio. Feed logical measures of stress recorded. Chicks were restriction of broiler breeder hens increased indi- hatched from each hen treatment and at day 7 vac- ces of stress in hens and resulted in offspring that cinated for infectious bronchitis virus (IBV) and have reduced growth rate and immune response at 16, 18, and 20 d old given an immune challenge in a sex-dependent way. Key words: broiler breeder, feed restriction developmental programming, immune response, meat chicken, stress © The Author(s) 2018. Published by Oxford University Press on behalf of the American Society of Animal Science. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact email@example.com Transl. Anim. Sci. 2018.2:263–271 doi: 10.1093/tas/txy064 1 2 The authors would like to acknowledge the Hi-Chick Breeder Corresponding author: firstname.lastname@example.org Company, Bethyl, SA, The Animal Biology Department, The Received March 22, 2018. University of Western Australia, ACE Laboratory Services, Accepted May 30, 2018. Bendigo, Victoria, and Associate Professor Kapil Chousalkar. Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018 264 Bowling et al. INTRODUCTION a commercial breeder facility in group pens. Hens were maintained at three different bodyweights, The concept that early life events affect health low, medium, and high, through feed restriction was first demonstrated during the Dutch famine on a commercial breeder hen diet. Hens were sep- (Barker, 2004). Early “events” occur during embry- arated into treatment groups at 24 wk of age and onic/fetal development, or early postnatal life and remained in these groups for the duration of the “impacts” can be metabolic, physiological, behav- experiment until 43 wk of age. Birds were fed once ioral, and immunological (Chmurzynska, 2010). a day at a level that would allow for a difference in The major environmental factor studied to date bodyweight between groups to be maintained. Feed has been maternal nutrition using intrauterine intake for hens was increased from 21 wk of age growth-restriction (IGUR) (Wu et al., 2004) and from an average of 112 g/bird/d to 31 wk of age dietary composition and level (Armitage et al., where birds were maintained at the maintenance 2005; Langley-Evans, 2006), with studies confirm - needed to maintain the desired bodyweights from ing the reprogramming effects of maternal diet each treatment. Low bodyweight’ hens were main- on progeny growth and health. Animals repro- tained on an average at 3.4 ± 0.1 kg and fed 140 g of grammed by early nutrition display “metabolic feed/hen/d, “medium-bodyweight” hens were main- syndrome,” which can include diabetes and hyper- tained on an average at 3.5 ± 0.1 kg and fed 145 g of tension (Langley-Evans, 2006; Elahi et al., 2009). feed/hen/d and “high-bodyweight” hens were main- Recently attention has been directed to the effects tained on an average at 3.9 ± 0.1 kg and fed 160 g of maternal stress reprogramming on immunolog- of feed/hen/d. Hens were weighed weekly to ensure ical functioning, with evidence of alterations in that correct bodyweights were maintained and feed immunity in offspring of stressed mothers in mul- intake of each group was adjusted to maintain bod- tiple species, from rodents (Kay, 1998) to livestock yweight differences between groups. (Couret et al., 2009; He et al., 2014) Eggs were collected over a 2-wk period from Although developmental programming stress each group of breeder hens. Eggs from each hen studies have been carried out in several species, treatment collected over the 2-wk collection period there is limited research in meat chickens. Mothers were randomized and incubated at 38° and 55% of meat chickens, breeder hens, are selected for humidity from days 0 to 15, and then 36.7°C and rapid, efficient growth of their progeny, leading 60% humidity until hatch at day 21 at Roseworthy to detrimental effects on their production of fer- Campus, The University of Adelaide. After hatch tile eggs. The subsequent management practice of viable chicks were weighed, ID tagged and placed feed restriction of hens leads to chronic hunger into group-rearing pens. Birds from each hen treat- and stress (de Jong et al., 2002; Mench, 2002; de ment group were placed in pens together with chicks Jong et al., 2003). Breeder hens are exposed to both from the same hen group over three replicates. under-nutrition and stress, likely affecting growth Standard husbandry procedures were followed and immunity of their offspring, through develop- with chicks placed in a shed at 25°C with heat mental programming. The aim of this study was to lamps in each pen and a light cycle of 23 h light for measure the impact on the growth and immunity of the first 24 h. From the second day, the light cycle progeny from breeder hens feed restricted to differ- was changed to 16 h light and the shed tempera- ing bodyweights. We hypothesized that hens kept ture adjusted accordingly. Chicks were fed ad libi- at the highest level of feed restriction and lowest tum a standard commercial meat bird starter diet bodyweight would show increased stress and have (Ridley Turkey and Meat Chicken Grower) until offspring with reduced growth and immunity. 3 wk of age and a commercial meat bird finisher diet (Ridley Turkey and Meat Chicken Finisher) MATERIALS AND METHODS until 6 wk old. All birds were given an ocular vac- cination for infectious bronchitis virus (IBV) at day 7, weighed weekly, and feed intake recorded. Animal Husbandry All animal use was approved by the ani- Hen Behavior Analysis mal ethics committees of The University of Breeder hens were observed daily over 1-h peri- Adelaide (S-2014-121) and The Department of ods in the morning during the 2-wk egg collection. Primary Industries and Regions, South Australia Behaviors were recorded using an ethogram at 30-s (PIRSA) (#14/14). A total of 36 Cobb 500 broiler intervals and the number of birds displaying each breeder hens were maintained in groups of 12 at Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Broiler breeder bodyweight affects progeny 265 behavior at each time point was recorded. The prior to weighing and sampling. Tissue samples of total numbers of observations for each behavior the duodenum, jejunum, ileum, liver, spleen, and and hen group were then added to give an overall bursa were then collected, snap frozen in liquid total. The behaviors used (Table 1) were adapted nitrogen, and stored at −80°C. from a previous study on breeder hen behavior (de Jong et al., 2003). Lipopolysaccharide Injections Half of the remaining chicks (n = 72) were Heterophil:Lymphocyte Counts given three injections of a lipopolysaccharide After blood collection, a drop of blood was (LPS) injection on alternate days, at 16, 18, and 20 placed onto a glass slide and smeared across the d of age. Birds in each treatment group received an slide to create a monolayer of cells. The slide was immune challenge injection of LPS Escherichia coli then fixed in 70% methanol for 60 s and allowed O55:B5 (Sigma-Aldrich) at a dose rate of 0.5 mg/kg to dry and later stained with Wright-Giemsa Stain bodyweight. Dose was determined after a review of using a Hematek Stain Pak (Bayer) Automatic the literature and the protocol was taken from Tan Stainer. All slides were counted at 40× magni- et al. (2014). The dose, however, was reduced to 0.5 fication three times by the same counter, under a from 1.0 mg/kg to reduce the risk of making the blinded analysis. Cells counted were lymphocytes, birds ill. Prior to injection, birds were weighed to heterophils, monocytes, basophils, and eosinophils determine dose rate and the injection site was dis- until a total of 100 cells were counted. A ratio of infected using 70% ethanol. The birds were given heterophils to lymphocyte cells was then calculated an intra-peritoneal injection beneath the keel bone, for each slide. 1 to 2 mm under the skin using a 23-gauge needle and 1-mL syringe. The remaining chicks (n = 74) in each hen treatment group did not receive the injec- Sampling tion of LPS. A blood sample was collected from 18 broiler progeny of each hen treatment group (n = 54). Yolk Immunoglobulin Y Samples were collected when birds were 21, 35, and 42 d old. Birds were sampled via the brachial Both egg yolk and serum samples were tested vein using a 23-gauge needle and 2-mL syringe for Immunoglobulin Y (IgY) concentration. Egg into 4-mL lithium heparin tubes and stored on ice. yolk samples were collected from 20 eggs from Samples were centrifuged at 2000 g for 5 min and low medium and heavy bodyweight hens (n = 60) plasma collected and stored at −20°C. over 1 wk. Medium hens were excluded from ana- Meat birds were grown until 42 d old and at lysis and only low and heavy hen yolks were tested, day 42, 69 birds (23 per hen group) were eutha- due to the larger difference in the hen feed intake nized. Birds were dissected and gross organ weight between these two groups. The eggs were weighed recorded for duodenum, jejunum, ileum, liver, and the yolk collected and stored at −20°C. To test heart, proventriculus, gizzard, spleen, and bursa. IgY concentrations in the yolk and serum sam- Duodenum, jejunum, ileum, gizzard, and proven- ples, a 96 well IgG (Chicken) ELISA kit was used triculus samples were opened and flushed of digesta (Abnova, Sapphire Bioscience) and standard kit procedure was followed. Table 1. Recorded broiler breeder hen behaviors For the egg yolk ELISA, IgY was first using an ethogram, at 30-s intervals, for 1 h, daily extracted using an adapted method (Hamel et al., over 2 wk of lay 2006). Briefly, the yolk was defrosted and twice the amount of Dulbecco’s PBS (Sigma-Aldrich) was Behavior category Observed behaviors added to the yolk and shaken vigorously. An equal Walking walking/running amount of chloroform (Sigma-Aldrich) was then Sitting sitting still added and mixed thoroughly to produce a thick Standing standing still emulsion which was centrifuged at 1,000 g for Peck drinker peck drinker (not drinking) Foraging pecking/scratching litter 30 min at room temperature. After centrifuging, Comfort preening, nibbling, stretching, and wing flapping three distinct layers were visible with IgY present Peck object peck object, peck cage (not including drinker) in the watery top layer, which was then removed Aggression peck another bird/fighting and aliquoted into 1-mL tubes and stored at −20°C Other any other observed behavior until analysis. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018 266 Bowling et al. Yolk and Plasma Corticosterone Organ weights were analyzed using a GLM, with day 42 bodyweight fitted into the model as a co-variate. Corticosterone was extracted from yolks A Fisher’s exact test was used to determine the sex (n = 40) using previously described methods (Cook ratio of the progeny from each hen bodyweight group. et al., 2009). Briefly, the egg yolk (~0.1 g) was taken A P value of <0.05 was deemed significant, with a and 0.5 mL of distilled water was added and vor- P value of >0.05 and <0.10 considered a trend. All texed until mixed. The mixture was extracted with data presented are the mean ± SEM. 3-mL hexane:diether (30:70 ratio) and vortexed and left to settle before snap freezing in an ethanol/ RESULTS dry ice bath. The supernatant was collected, dried, and 1 mL of ethanol was added to the samples Hen Behavior which were frozen at −80°C overnight. The samples were centrifuged the next day and the supernatant Forage and pecking behaviors differed between taken and dried once more. The samples were then hen bodyweight groups (P < 0.05) (Table 2). Hens thawed, resuspended in 500 µL of phosphate buffer kept at the lowest bodyweight were observed forag- saline, and analyzed. ing the least number of times (4.8 ± 2.7) compared Extracted yolk and plasma samples from with medium (23.6 ± 2.8) and high bodyweight progeny birds at 23 (n = 53) and 42 d old (n = 54) hens (13.4 ± 3.1). Low bodyweight hens also were analyzed for corticosterone concentrations. pecked objects in the cage more (184 ± 6.6) than Samples were analyzed at the University of Western medium (137.7 ± 6.8) and high bodyweight hens Australia, Animal Biology Department using a val- (132. 8 ± 7.5) (P < 0.05). idated Radio Immuno Assay Corticosterone 125I RIA KIT (MP Biomedical, Orangeburg, NY). Hen Heterophil:Lymphocyte Counts IBV Antibody Analysis The H:L counts of white blood cells at 31 wk of age approached statistical significance ( P = 0.06). Low Plasma samples collected at 35 d of age from bodyweight hens had a greater H:L ratio (1.03 ± 0.1) offspring of heavy (n=15) and low (n =17) body- compared with hens maintained at medium weight hens were analyzed for IBV antibodies, after (0.67 ± 0.1) and high bodyweights (0.59 ± 0.1). vaccination at day 7. Samples were analyzed by ACE Laboratory Services (Bendigo, Victoria) using Yolk and Progeny IgY an IBV (Ab) ELISA (BioCheck). No statistical significance ( P > 0.05) was found Statistical Analysis in egg yolk IgY concentration (ng/mL) in eggs taken from heavy (64.6 ± 6.6) and low bodyweight hens Statistical analysis was performed using the IBM (66.5 ± 6.7). There was also no statistical difference SPSS statistical program version 21. Hen behavior, (P > 0.05) in blood serum IgY (ng/mL) taken on yolk IgY concentration, plasma IBV titres, yolk and day 23 from progeny of low (12.6 ± 3.0) and high plasma corticosterone, and H:L cell counts were ana- bodyweight hens (13.9 ± 3.0). lyzed using a general linear model (GLM) with fixed effects of hen bodyweight, gender, and LPS treatment Progeny Sex Ratio and interactions fitted into the model. Bodyweight was analyzed for each bird using repeated meas- The sex ratio of progeny from low and heavy ures with the same parameters fitted into the model. bodyweight hens was significantly different Table 2. Total number of times hens maintained at a low, medium, and heavy bodyweight were observed displaying foraging and pecking behaviors, using an ethogram with observations taken every 30 s, over 1 h, daily for 2 wk Hen weight Forage SEM P-value Peck SEM P-value a a Low 4.8 2.7 0.011 184.0 6.6 <0.001*** b b Medium 23.6 2.8 0.007 137.7 6.8 0.156 c b High 13.4 3.1 0.011 132.8 7.5 <0.001*** Values are means ± SEM, n = 36. Means in a column with superscripts differ, P < 0.05 Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Broiler breeder bodyweight affects progeny 267 (P < 0.048). A greater proportion of males were bodyweight hens. There was a trend towards signif- hatched from heavy bodyweight hens (n = 26), com- icance (P = 0.094) in the interaction of hen bod- pared with lower bodyweight hen offspring (n = 18). yweight*sex, in plasma corticosterone (ng/mL) in Female hatch rates were opposite and were greater the offspring at 42 d old between males and females in lower bodyweight hens (n = 19) and reduced in from high and low bodyweight hens. The oppo- heavy bodyweight hen progeny (n =11) (Figure 1). site was found to day 23, with corticosterone levels were elevated in females from low bodyweight hens (82.5 ± 11.8) compared with females from high bod- Yolk and Plasma Corticosterone yweight hens (50.3 ± 13.6). In males, plasma cor- A trend towards significance ( P = 0.086) was ticosterone levels were reduced in those from low found in yolk corticosterone (ng/g) between off- bodyweight hens (58.8 ± 7.8) compared with male spring of low (90.8 ± 17.7), medium (74.8 ± 21.3), from high (61.3 ± 9.6) bodyweight hens (Figure 2). and high (87.3 ± 18.1) hens. The yolk cortico- sterone concentrations (ng/g) between low and Progeny Growth medium bodyweight hens was significantly differ - ent (P = 0.045). A significant three-way interaction ( P < 0.001) At 23 d of age, there was no significant differ - was found in bodyweight of the progeny, of hen ence (P > 0.05) in plasma corticosterone (ng/mL) bodyweight, sex, and age. This interaction showed in offspring from low (89.4 ± 10.3), medium an effect of decreased bodyweight (g) in male prog- (95.8 ± 11.2), and high (120.4 ± 17) bodyweight eny from low bodyweight hens (2678.9 ± 52.9) hens. There was a trend towards a significant differ - compared with males from heavy bodyweight hens ence in plasma corticosterone (ng/mL) (P = 0.065) (2906.3 ± 46.1) at 42 d of age (Figure 3). in the interaction between males and females from high and low bodyweight hens. Females from high Immunity Challenge and Response to LPS bodyweight hens had increased corticosterone A significant difference ( P = 0.05) was found (139.8 ± 31) compared with females from low body- at day 35 in plasma antibodies to IBV between weight hens (71.4 ± 13.9). In males, the opposite was progeny from heavy (n = 15) and low bodyweight seen with decreased corticosterone in males from hens (n = 17). Antibody titers to the vaccination high bodyweight hens (101 ± 9.8) compared with at day 7 were elevated in progeny from heavy hens males from low bodyweight hens (107.5 ± 13.9). (492.7 ± 76.1) compared with progeny from low At 42 d of age, there was also no significant bodyweight hens (287.3 ± 70.1), as seen in Figure 4. difference (P > 0.05) in plasma corticosterone lev- Heterophil:lymphocyte (H: L) ratios at 23 els (ng/mL) between offspring of low (70.7 ± 7.1), d of age showed significant differences between medium (57.3 ± 9.3), and high (55.8 ± 8.3) males and females from heavy hens (P < 0.05). Females from heavy hens had a significantly greater H: L ratio (0.79 ± 0.15) than males from Figure 2. Plasma corticosterone (ng/mL) at 42 d of age in males Figure 1. Sex ratio of broiler progeny at hatch from low and heavy and females from low (n = 13) and high (n = 11) bodyweight hens. bodyweight breeder hens. Significance was evaluated using a chi- Values are mean ± SEM. Significance was evaluated using a two-way square, Fischer’s exact test with significance at P < 0.05. ANOVA. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018 268 Bowling et al. Figure 5. Heterophil:lymphocyte ratio of males and females from Figure 3. Bodyweight (g) of male progeny from low, medium, and low, medium, and heavy bodyweight hens. Values are means ± SEM heavy hens from hatch (day 0) until 42 d of age. Weight is mean ± (n = 36). Significance was evaluated using a one-way ANOVA with sig - SEM. Significance was evaluated using a repeated measures model nificance at P < 0.05. Labeled means without a common letter differ, with significance at P < 0.05. P < 0.05. females (860 ± 27.2). Males from heavy hens were not affected in the same way, with males injected with LPS weighing the same (848.5 ± 18.5) as male controls (873.3 ± 19.3). At dissection at 42 d old, there was a significant difference in spleen weight (P < 0.05) with body- weight at day 42 fitted as a co-variate. Progeny from heavy bodyweight hens had significantly heavier gross spleen weight at day 42 (3.0 ± 0.2) compared with progeny of medium (2.4 ± 0.2) and low body- weight hens (2.3 ± 0.2). DISCUSSION Figure 4. Plasma IBV antibody titers at 35 d old in progeny of low (n = 17) and heavy hens (n = 15). Values are means ± SEM. Significance Hen Feed Restriction and Stress was evaluated using a one-way ANOVA with significance at P < 0.05. Hens maintained at a low bodyweight from heavy hens (0.32 ± 0.07) as well as females from 24 wk old displayed decreased foraging behavior both low (0.38 ± 0.11) and medium bodyweight and increased object pecking. Increased pecking hens (0.28 ± 0.11). There was no difference seen and reductions in comfort behaviors (such as for- between males from heavy (0.32 ± 0.07), medium aging) can indicate chronic hunger in breeder hens, (0.32 ± 0.08), and low bodyweight hens (0.42 ± 0.08) with correlations between these behaviors and other (Figure 5). measurements of hunger such as feed intake moti- There was a significant difference ( P < 0.05) vation tests and glucose/NEFA ratio (de Jong et al., in bodyweight (g) on day 21 between all prog- 2003). These behaviors, indicative of chronic hun- eny injected with LPS (798 ± 8.7) and controls ger, were accompanied by changes in the ratio of (835.7 ± 8.7). After injection with LPS, a significant heterophil to lymphocytes in the blood, an accepted difference in bodyweight was observed between indicator of stress in poultry (Müller et al., 2011). males and females on day 21 (P < 0.05). Female We cannot directly attribute stress in the hens to bodyweights (g) were lower after LPS injection low feed intake per se as there may be some other (786.45 ± 11.7) compared with males that received component of low bodyweight that is the trigger to LPS (842.8 ± 9.2). stress, but whatever it is, it must ultimately relate to There was also a significant interaction of sex - low intake. *hen bodyweight on day 21 bodyweight (P < 0.05). Yolk corticosterone levels can reflect plasma Females hatched from heavy hens were affected corticosterone levels in hens (Henriksen et al., 2011). by the LPS challenge, with those given the LPS Surprisingly, hens maintained at a medium level of injection weighing less (755.3 ± 27.2) than control feed restriction had the lowest yolk corticosterone Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Broiler breeder bodyweight affects progeny 269 concentration. These same hens also showed exposure (Hayward et al., 2006) as well as behavior increased foraging behavior, and this together with changes in males (Goerlich et al., 2012). It is possi- the yolk corticosterone suggests that medium bod- ble that males may be more sensitive to changes in yweight hens were the least stressed, followed by corticosterone levels during development and other heavy hens. This is likely due to an increased level maternal changes (Rubolini et al., 2005a), and per- of feed given to these birds, compared with the low- haps, this is why only male growth was affected. est bodyweight hens. Progeny Immunity and Response to LPS Challenge IgY Maternal Transfer Hen bodyweight had a significant effect on the No difference was found in yolk IGY anti- antibody titer at 35 d of age of their progeny to the bodies between hen treatments. There was also no IBV vaccine at day 7. Antibody levels were found significant difference between progeny of hens in to be elevated in progeny from high bodyweight plasma IgY, and therefore, it can be assumed that hens, compared with those from low bodyweight differences in progeny were not due to the transfer hens. This is a significant result as it demonstrates of IgY antibodies from the hen to the chick. the impact of the hen bodyweight on the ability of the progeny to mount an immune response to a vaccination. The increased antibody titers in prog- Progeny Sex Ratio eny of high bodyweight hens suggest an enhanced immune response of these birds in response to Sex ratio of chicks hatched was affected by hen the vaccination, compared with progeny of low bodyweight, with an increase in males hatched from bodyweight hens. heavy bodyweight hens. One possible reason behind Spleen weight relative to bodyweight was this is the ability of avian species to modify hatch- also increased in progeny from heavy hens and ling sex ratio via changes in production of gonadal although spleen weight as a measure of immunity steroids, resulting in changes in egg hormone con- is debatable may have affected the antibody titers centrations (Henriksen et al., 2011). Testosterone is to IBV. A reduced spleen weight can be an effect thought to be one such hormone behind this abil- of increased stress and corticosterone (Post, 2003) ity to manipulate sex ratios, with increases in yolk and although not significant, corticosterone within testosterone linked to increases in male born off- the yolk was slightly elevated in the low bodyweight spring (Veiga et al., 2004; Rubolini et al., 2005b). hens. There is therefore the potential that there was As testosterone and corticosterone levels can be an elevated corticosterone or other glucocorticoid influenced by one another; corticosterone levels elevated exposure within the low bodyweight eggs. can be opposite to testosterone in chicken egg yolk These hens did also have elevated H:L counts and (Henriksen et al., 2011). The decreased cortico- behaviors indicative of stress, which could have sterone within the yolks from heavy hens may there- affected the immunity of their offspring, including fore suggest that testosterone levels were elevated spleen size and weight. This reduced spleen weight within these eggs, resulting in increased male hatch- may then have gone on to reduce their immune abil- lings; although testosterone was not measured in ity as the spleen in avians is a storage organ of lym- this study, it should be considered in future work. phocytes (Smith and Hunt, 2004) and their ability to produce the same amount of antibodies as birds Progeny Growth from high bodyweight hens. Hen bodyweight did significantly affect the The impact of maternal stress and elevated growth of their offspring, but only in males during glucocorticoids has been demonstrated in mul- the final week of growth, with males from low bod - tiple species. In rodents, stressed mothers have yweight hens significantly lighter than males from given birth to offspring with decreased leuko- heavy mothers. Yolk corticosterone was increased cyte counts, reduced B cell proliferation (Kay, in low bodyweight hens, and elevated corticosterone 1998; Llorente et al., 2002), and reduced anti- in hens has been previously linked to decreased bodies (Gorczynski, 1992; Sobrian et al., 1997), growth in their offspring (Janczak et al., 2006; Shini as seen in this study. Similar findings have also et al., 2009; Ahmed et al., 2014), and could explain been shown in primates (Coe et al., 1999), with the reduced growth in males from low bodyweight decreased T cell response to antigens in offspring hens. Previous avian research has also found of stressed mothers and decreased white blood reduced growth only in males after corticosterone cells in piglets from stressed sows (Couret et al., Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018 270 Bowling et al. 2009). Therefore, the impact of maternal stress on Reduced bodyweight through feed restriction the immunity of the offspring has been demon- in broiler breeder hens appears to induce a stress strated across other species and is likely to occur response with changes in behavior and H:L counts, in meat birds, as shown in this study and although affecting the progeny, possibly related to elevated the link between larger spleens and increased corticosteroid levels in the yolk of the developing immunity has not been definitively shown in avi - embryo. Progeny from these hens was affected in ans (Smith and Hunt, 2004). Spleen size could several ways in a sex-specific way. Males from less have been affected by maternal stress and possi- feed-restricted hens grew at a greater rate later in bly affected the antibody production in response life and females from these hens mounted a stronger to the vaccine. Overall, progeny from less feed-re- immune response to an LPS challenge compared stricted heavy bodyweight hens was exhibiting an with progeny from hens with heavier feed restric- expected response and may be more sensitive to tion. The results of this study have serious implica- an immune threat than birds from lower body- tions for the chicken meat industry both in terms of weight hens, under increased feed restriction. the welfare of feed-restricted hens but also for the Overall LPS-injected birds had a reduction in health and productivity of the progeny meat bird. bodyweight at day 21, which might be expected as Maintaining breeder hens at a heavier bodyweight the birds partitioned nutrients to mount an immune may therefore mean that hens are less stressed and response (Klasing, 2007). Voluntary feed intake did could result in improved growth in male broilers not appear to alter between treatments; however, the and immunity in females as well as overall immune challenge was at a low dose and showed no effect on response to vaccination. bird behavior or feeding. If the challenge dose was elevated, it is likely that feed intake would decrease. LITERATURE CITED Differences in response between birds from low Ahmed, A. A., W. Ma, Y. Ni, S. Wang, and R. Zhao. 2014. and heavy bodyweight hens were also found, with Corticosterone in ovo modifies aggressive behaviors increased plasma corticosterone in LPS-challenged and reproductive performances through alterations birds from heavy hens. An increased plasma cor- of the hypothalamic-pituitary-gonadal axis in the chicken. Anim. Reprod. Sci. 146:193–201. doi:10.1016/j. ticosterone concentration might also be expected anireprosci.2014.02.013 as pro-inflammatory cytokines are elevated, along Armitage, J. A., P. D. Taylor, and L. Poston. 2005. Experimental with corticosterone (Lu et al., 2008). models of developmental programming: consequences of Differences in immune response were also exposure to an energy rich diet during development. J. found within gender between progeny from dif- Physiol. 565(Pt 1):3–8. doi:10.1113/jphysiol.2004.079756 Barker, D. J. 2004. The developmental origins of well-being. ferent bodyweight hens. Females from heavy hens Philos. Trans. R. Soc. Lond. B. Biol. Sci. 359:1359–1366. challenged with LPS were significantly different doi:10.1098/rstb.2004.1518 from other LPS females, with reduced growth at Chmurzynska, A. 2010. Fetal programming: link between early day 21 after the challenge, increased H:L ratio, and nutrition, DNA methylation, and complex diseases. Nutr. increased plasma corticosterone. Males from heavy Rev. 68:87–98. doi:10.1111/j.1753-4887.2009.00265.x hens given LPS showed a similar increase in cor- Coe, C. L., G. R. Lubach, and J. W. Karaszewski. 1999. Prenatal stress and immune recognition of self and non- ticosterone later at day 42, suggesting they may be self in the primate neonate. Biol. Neonate 76:301–310. slower to respond than the females. doi:10.1159/000014172 Reduced bodyweight and increased cortico- Cook, N. J., R. Renema, C. Wilkinson, and A. L. Schaefer. sterone are part of the immune response to the 2009. Comparisons among serum, egg albumin LPS. The elevation in H:L ratio also suggests the and yolk concentrations of corticosterone as bio- markers of basal and stimulated adrenocortical mounting of an immune response, as heterophils activity of laying hens. Br. Poult. Sci. 50:620–633. are part of the avian immune response (Shini et al., doi:10.1080/00071660903147424 2010) and are also elevated with increased cortico- Couret, D., A. Jamin, G. Kuntz-Simon, A. Prunier, and sterone (Shini et al., 2008). These changes were not E. Merlot. 2009. Maternal stress during late gestation has seen in females from low and medium bodyweight moderate but long-lasting effects on the immune system hens, which indicates that these birds were not of the piglets. Vet. Immunol. Immunopathol. 131:17–24. doi:10.1016/j.vetimm.2009.03.003 mounting the same immune response. Therefore, Elahi, M. M., F. R. Cagampang, D. Mukhtar, F. W. Anthony, the heavy hen females seem more able to respond S. K. Ohri, and M. A. Hanson. 2009. Long-term mater- to immune problems and although the LPS was nal high-fat feeding from weaning through pregnancy and low and did not cause any visible illness, these birds lactation predisposes offspring to hypertension, raised may be more likely to be able to defend against an plasma lipids and fatty liver in mice. Br. J. Nutr. 102:514– 519. doi:10.1017/S000711450820749X immune challenge. Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018 Broiler breeder bodyweight affects progeny 271 Goerlich, V. C., D. Nätt, M. Elfwing, B. Macdonald, Mench, J. A. 2002. Broiler breeders: feed restriction and welfare. and P. Jensen. 2012. Transgenerational effects of World’s Poultry Science Journal 58: 23–29. doi:10.1079/ early experience on behavioral, hormonal and gene WPS20020004 expression responses to acute stress in the precocial Müller, C., S. Jenni-Eiermann, and L. Jenni. 2011. Heterophils/ chicken. Horm. Behav. 61:711–718. doi:10.1016/j. lymphocytes-ratio and circulating corticosterone do yhbeh.2012.03.006 not indicate the same stress imposed on Eurasian Gorczynski, R. M. 1992. Conditioned stress responses by preg- kestrel nestlings. Functional Ecology 25: 566–576. nant and/or lactating mice reduce immune responses of doi:10.1111/j.1365-2435.2010.01816.x their offspring after weaning. Brain. Behav. Immun. 6:87– Post, J., J. M. Rebel, and A. A. ter Huurne. 2003. Physiological 95. doi:10.1016/0889-1591(92)90062-S effects of elevated plasma corticosterone concentrations in Hamel, K. R., S. C. Burgess, I. Y. Pevzner, and G. F. Erf. 2006. broiler chickens. An alternative means by which to assess Maternal antibody transfer from dams to their egg yolks, the physiological effects of stress. Poult. Sci. 82:1313– egg whites, and chicks in meat line chickens. Poult. Sci. 1318. doi:10.1093/ps/82.8.1313 85(8):1364–1372. doi:10.1093/ps/85.8.1364 Rubolini, D., M. Romano, G. Boncoraglio, R. P. Ferrari, Hayward, L. S., J. B. Richardson, M. N. Grogan, and R. Martinelli, P. Galeotti, M. Fasola, and N. Saino. 2005a. J. C. Wingfield. 2006. Sex differences in the organiza - Effects of elevated egg corticosterone levels on behavior, tional effects of corticosterone in the egg yolk of quail. growth, and immunity of yellow-legged gull (larus micha- Gen. Comp. Endocrinol. 146:144–148. doi:10.1016/j. hellis) chicks. Horm. Behav. 47:592–605. doi:10.1016/j. ygcen.2005.10.016 yhbeh.2005.01.006 He, Z. X., Z. H. Sun, W. Z. Yang, K. A. Beauchemin, S. X. Rubolini, D., M. Romano, R. Martinelli, and N. Saino. 2005b. Tang, C. S. Zhou, X. F. Han, M. Wang, J. H. Kang, and Effects of elevated yolk testosterone levels on survival, Z. L. Tan. 2014. Effects of maternal protein or energy growth and immunity of male and female yellow-leg- restriction during late gestation on immune status and ged gull chicks. Behav. Ecol. Sociobiol. 59: 344–352. responses to lipopolysaccharide challenge in postnatal doi:10.1007/s00265-005-0057-0 young goats. J. Anim. Sci. 92:4856–4864. doi:10.2527/ Shini, S., P. Kaiser, A. Shini, and W. L. Bryden. 2008. Biological jas.2014-7904 response of chickens (gallus gallus domesticus) induced Henriksen, R., T. G. Groothuis, and S. Rettenbacher. 2011. by corticosterone and a bacterial endotoxin. Comp. Elevated plasma corticosterone decreases yolk testos- Biochem. Physiol. B. Biochem. Mol. Biol. 149:324–333. terone and progesterone in chickens: linking maternal doi:10.1016/j.cbpb.2007.10.003 stress and hormone-mediated maternal effects. PLoS One Shini, S., A. Shini, and G. R. Huff. 2009. Effects of chronic 6:e23824. doi:10.1371/journal.pone.0023824 and repeated corticosterone administration in rearing Janczak, A. M., B. O. Braastad, and M. Bakken. 2006. chickens on physiology, the onset of lay and egg pro- Behavioural effects of embryonic exposure to cortico- duction of hens. Physiol. Behav. 98:73–77. doi:10.1016/j. sterone in chickens. Appl. Anim. Behav. Sci. 96: 69–82. physbeh.2009.04.012 doi:10.1016/j.applanim.2005.04.020 Shini, S., A. Shini, and P. Kaiser. 2010. Cytokine and chemok- de Jong, I. C., A. S. van Voorst, and H. J. Blokhuis. 2003. ine gene expression profiles in heterophils from chick - Parameters for quantification of hunger in broiler ens treated with corticosterone. Stress 13:185–194. breeders. Physiol. Behav. 78:773–783. doi:10.1016/ doi:10.3109/10253890903144639 S0031-9384(03)00058-1 Smith, K. G., and J. L. Hunt. 2004. On the use of spleen mass de Jong, I. C., S. van Voorst, D. A. Ehlhardt, and H. J. Blokhuis. as a measure of avian immune system strength. Oecologia 2002. Effects of restricted feeding on physiological stress 138:28–31. doi:10.1007/s00442-003-1409-y parameters in growing broiler breeders. Br. Poult. Sci. Sobrian, S. K., V. T. Vaughn, W. K. Ashe, B. Markovic, 43:157–168. doi:10.1080/00071660120121355 V. Djuric, and B. D. Jankovic. 1997. Gestational expos- Kay, G., N. Tarcic, T. Poltyrev, and M. Weinstock. 1998. ure to loud noise alters the development and postnatal Prenatal stress depresses immune function in rats. responsiveness of humoral and cellular components of Physiol. Behav. 63:397–402. doi:10.1016/S0031-9384(97) the immune system in offspring. Environ. Res. 73:227– 00456-3 241. doi:10.1006/enrs.1997.3734 Klasing, K. C. 2007. Nutrition and the immune system. Br. Tan, J., S. Liu, Y. Guo, T. J. Applegate, and S. D. Eicher. Poult. Sci. 48:525–537. doi:10.1080/00071660701671336 2014. Dietary L-arginine supplementation attenuates Langley-Evans, S. C. 2006. Developmental programming lipopolysaccharide-induced inflammatory response in of health and disease. Proc. Nutr. Soc. 65: 97–105. broiler chickens. Br. J. Nutr. 111:1394–1404. doi:10.1017/ doi:10.1079/PNS2005478 S0007114513003863 Llorente, E., M. L. Brito, P. Machado, and M. C. González. Veiga, J. P., J. Viñuela, P. J. Cordero, J. M. Aparicio, and V. Polo. 2002. Effect of prenatal stress on the hormonal response 2004. Experimentally increased testosterone affects social to acute and chronic stress and on immune parame- rank and primary sex ratio in the spotless starling. Horm. ters in the offspring. J. Physiol. Biochem. 58:143–149. Behav. 46:47–53. doi:10.1016/j.yhbeh.2004.01.007 doi:10.1007/BF03179851 Wu, G., F. W. Bazer, T. A. Cudd, C. J. Meininger, and Lu, Y. C., W. C. Yeh, and P. S. Ohashi. 2008. LPS/TLR4 T. E. Spencer. 2004. Maternal nutrition and fetal signal transduction pathway. Cytokine 42:145–151. development. J. Nutr. 134:2169–2172. doi:10.1093/ doi:10.1016/j.cyto.2008.01.006 jn/134.9.2169 Translate basic science to industry innovation Downloaded from https://academic.oup.com/tas/article-abstract/2/3/263/5033840 by Ed 'DeepDyve' Gillespie user on 31 July 2018
Translational Animal Science – Oxford University Press
Published: Sep 1, 2018
Access the full text.
Sign up today, get DeepDyve free for 14 days.