Effects of Environmental Enrichments on Welfare and Hepatic Metabolic Regulation of Broiler Chickens

Abstract

The aims of this study were to find suitable environmental enrichment (EE) and evaluate the combined effect of two EEs, variable light intensity (VL) lighting program and EH, on mental health and hepatic metabolic regulation in commercial broilers. To find the advantageous EEs for broilers, three different EEs (board, hut, and ramp) were tested in trial 1. EEs were placed and the engagement of birds to EEs, dustbathing behavior, and daily physical activity were observed. Birds treated with huts showed higher engagement than the board- or ramp-treated birds (p < 0.05). The results of dustbathing behavior and daily physical activity indicated that the environmental hut (EH) is the most favorable enrichment for broilers. In the second trial, to test the effect of EHs on mental health and hepatic metabolic conditions, the brain and liver were sampled from the four treatment birds (20 lx_Con, 20 lx_Hut, VL_Con and VL_Hut) on day 42. The lower expression of TPH2 (tryptophan hydroxylase 2) of VL_Hut birds than those of VL_Con and 20 lx_Hut treated birds suggests the combining effect of EHs with the VL lighting program on the central serotonergic homeostasis of broilers. Reduced expressions of TH (tyrosine hydroxylase), GR (glucocorticoid receptor), BDNF (brain-derived neurotrophic factor) of VL_Hut treated birds compared to those of VL_Con and 20 lx_Hut birds suggest lower stress, stress susceptibility, and chronic social stress in VL_Hut treated birds. The expression of CPT1A (carnitine palmitoyl transferase 1) increased over three-fold in the liver of VL_Con birds compared to 20 lx_Con birds (p < 0.05). EHs treatment in VL birds (VL_Hut) significantly decreased CPT1A but not in 20 lx birds (20 lx_Hut). The expression of ACCα (acetyl-CoA carboxylase alpha) was significantly decreased in VL_Con birds compared to 20 lx_Con birds. There was no significant difference in the hepatic FBPase (fructose-1,6-bisphosphatase), GR, and 11β-HSD1 (11 β-hydroxysteroid dehydrogenease-1) expression between 20 lx_Con and VL_Con birds, but EHs significantly stimulated GR in 20 lx_Hut birds, and stimulated FBPase and 11β-HSD1 expression in the VL_Hut birds compared to 20 lx_Con birds, suggesting that the VL lighting program reduced fatty acid synthesis and increased fatty acid β-oxidation in the broilers' liver and VL_Hut improved the hepatic de novo glucose production. Taken together, the results suggest that the stimulated voluntary activity by EHs in the light-enriched broiler house improved mental health and hepatic metabolic function of broilers and may indicate that the improved hepatic metabolic function contributes to efficient nutritional support for broilers.

Keywords: BDNF; dopamine; enrichment hut; hepatic fatty acid; serotonin; variable light intensity; welfare.

Figure 1

Effects of the three different environment enrichments (board, hut, and ramp) on engagement of birds at different ages. (A–C) Three commercially available enrichments placed in trial 1, 20 lx and VL houses. Enrichment dimensions: Board; 10.2 cm (diameter) × 182.9 cm (long), Hut; 35.6 cm (wide) × 76.2 cm (long) × 35.6 cm (height), Ramp; 61.0 cm (wide) × 91.4 cm (long) × 30.5 cm (height). (D–F) Weekly number of engaged birds was observed on day 28, 35, and 42 for each enrichment. Data (mean ± SEM) were compared among treatments. Different lower-case letters above the bars denote significant differences (p < 0.05) among groups.

Figure 2

Effects of the three different enrichments (board, hut, and ramp) on the number of dustbathing holes in different light condition and ages. In each section of trial 1, 20 lx houses (A) and VL houses (B), dustbathing holes as the evidence of dustbathing behavior were counted at 8, 15, and 22 days of age. Dustbathing holes were observed in nine parts of each section and the number of holes per 5 m² was determined. Data (mean ± SEM) were compared among treatments. Different lower-case letters above the bars denote significant differences (p < 0.05) among groups.

Figure 3

Effects of the different environmental enrichments (board, hut, and ramp) on daily physical activity. In each section of trial 1 VL houses, an activity tracker, Animo, was installed on birds using harness at 43 days of age and uninstalled at 48 days of age (n = 8 birds/trt, 4 birds/section, 2 VL houses). Average daily activity (calorie consumption) for each bird from day 44 to day 47 was obtained. Data (mean ± SEM) were compared among treatments (control, board, hut, and ramp). Different lower-case letters above the bars denote significant differences (p < 0.05) among groups.

Figure 4

Sagittal view of dissection area of the chicken midbrain (Ventral Tegmental Area). Dimensions of dissected tissue are coronally 3–3.5 mm (W) × 2–3 mm (H) × 1–1.2 mm (L) for VTA. The thickness (W, H, and L) was adjusted proportionally from young birds to older birds based on brain size and structure. Abbreviations used: AM: anterior medial hypothalamic nucleus; CA: anterior commissure; Cb: cerebellum; CO: optic chiasma; CP: posterior commissure; DMA: dorsomedial nucleus; EW: Edinger–Westphal nucleus; FLM: medial longitudinal fasciculus; FV: ventral fasciculus; IH: inferior hypothalamic nucleus; IN: infundibular hypothalamic nucleus; LSO: lateral septal organ; MM: medial mammillary nucleus; MnX: nucleus motorius dorsalis nervi vagi; NC: caudal neostriatum; NH: neurohypophysis; NHpC: nucleus of the hippocampal commissure; NIII: oculomotor nerve; nIV: trochlear nerve nucleus; nXII: hypoglossal nerve nucleus; OI: inferior olivary nucleus; OMd: dorsal oculomotor nucleus; P: pineal gland; POM: medial preoptic nucleus; PVN: paraventricular nucleus; RPgc: nucleus of caudal pontine reticular gigantocellular; Ru: red nucleus; SCE: stratum cellular externum; TSM: septopallio-mesencephalic tract; Top VMN: ventromedial hypothalamic nucleus.

Figure 5

Expression changes of (A) TPH2, (B) TH (the rate-limiting enzyme of dopamine biosynthesis), (C) glucocorticoid receptor (GR), and (D) brain-derived neurotropic factor (BDNF) mRNA in the ventral tegmental area (VTA) of birds at 42 days of age. Brains of birds were sampled on day 42 (n = 12/section, 4 sections/house). The VTA of the brainstem from each bird was dissected as described in Materials and Methods. Total RNA was extracted and used for RT-qPCR. Data were set as the relative fold changes of expression levels using the ΔΔCt method with GAPDH and β-actin as internal controls. Data (mean ± SEM) were expressed from a value set for 1.0 for 20 lx_Con birds for each gene. Different lower-case letters above the bars denote significant differences (p < 0.05) among groups.

Figure 6

Expression changes of hepatic (A) L-CPT1A (liver carnitine palmitoyl transferase 1), (B) L-ACCα (liver acetyl-CoA carboxylase alpha), (C) L-FBPase (liver Fructose -1,6-bisphosphatase), (D) L-GR (liver glucocorticoid receptor), and (E) L-11β-HSD1 (liver 11 β-hydroxysteroid dehydrogenease-1) genes and (F) VTA Opn4 gene. Total RNA was extracted from liver and macro dissected VTA tissues and used for real time RT-qPCR. Data were set as the relative fold changes of expression levels using the ΔΔCt method with GAPDH, β-actin, and 18S as internal controls. Data (mean ± SEM) were expressed from a value set for 1.0 for 20 lx_Con birds at 14 days of age. Different lower-case letters above the bars denote significant differences (p < 0.05) among groups.