Chick neonatal environment: the presence of a hen, not hatching system, promotes cecal microbiota development and induces limited long-term effects on immunity and redox balance.

This study investigated how hatching environment and early-life exposure to an adult hen influence gut microbiota development, immune function, and redox status in broiler chicks. Male chicks were hatched either on-farm (OFH) or in a conventional hatchery (CH), with or without the presence of an adult hen for the first 15 days post-hatching (CH+H, OFH+H). An additional group received antibiotic treatment during this period (CH+AB). At 27 days post-hatching, the chicks faced suboptimal conditions (transport, temperature fluctuations, and increased density) and were vaccinated against Gumboro disease to test their resilience. Cecal bacterial gene communities and immune gene expression in the bursa of Fabricius and cecal tonsils were assessed at 20 and 56 days of age. Plasma immune, metabolic, and redox status were evaluated at 27, 40, and 56 days. At 20 days, hen contact promoted the development of the cecal microbiota, characterized by increased relative abundances of Bacteroides, Prevotellaceae UCG-001, Parabacteroides, Mucispirillum, Desulfovibrio, Succinatimonas, Olsenella, and Sutterella. In OFH chicks, hen contact reduced cecal IgA concentrations. Conversely, in CH+AB chickens, the bacterial diversity diminished, favoring Escherichia-Shigella dominance, and TNF gene expression was increased in the cecal tonsils. While the hatching system alone had no effect on microbiota, it acted synergistically with hen contact and further enhanced microbiota maturity. At 56 days, most early observed differences in microbiota composition had disappeared. However, in CH+H chickens, IgA gene expression decreased in the bursa of Fabricius and CD40 mRNA expression increased in the cecal tonsils. In OFH+H chickens, the lipid oxidative status was reduced in favor of a better redox status compared to OFH chickens. In conclusion, the contact of chicks with a hen during the start-up period had a transient but significant effect on gut microbiota development during the initial colonization window. Although most effects diminished over time, lasting changes in immune function and redox status warrant further investigation to uncover the long-term health benefits of neonatal environmental enrichment in poultry.