The Glutamatergic System Regulates Feather Pecking Behaviors in Laying Hens Through the Gut–Brain Axis

Feather pecking (FP) is a significant welfare and economic problem in laying hen husbandry. While there is growing evidence that the glutamatergic system plays a crucial role in regulating FP behavior, the biological mechanisms remain unclear, largely due to the limited uptake of peripheral glutamat...

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Main Authors: Xiliang Yan, Chao Wang, Yaling Li, Yating Lin, Yinbao Wu, Yan Wang
Format: Article
Language:English
Published: MDPI AG 2025-04-01
Series:Animals
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Online Access:https://www.mdpi.com/2076-2615/15/9/1297
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author Xiliang Yan
Chao Wang
Yaling Li
Yating Lin
Yinbao Wu
Yan Wang
author_facet Xiliang Yan
Chao Wang
Yaling Li
Yating Lin
Yinbao Wu
Yan Wang
author_sort Xiliang Yan
collection DOAJ
description Feather pecking (FP) is a significant welfare and economic problem in laying hen husbandry. While there is growing evidence that the glutamatergic system plays a crucial role in regulating FP behavior, the biological mechanisms remain unclear, largely due to the limited uptake of peripheral glutamate across the blood–brain barrier (BBB). Here, we applied a multi-omics approach combined with physiology assays to answer this question from the perspective of the gut–brain axis. A total of 108 hens were randomly assigned to two groups (treatment and control) with six replicates each, and the treatment group was subjected to chronic environmental stressors including re-housing, noise, and transport. We found that chronic exposure to environmental stressors induced severe FP, accompanied by reduced production performance and increased anxiety- and depression-related behaviors, compared to controls. In addition, the immune system was potentially disrupted in FP chickens. Notably, gut microbiota diversity and composition were significantly altered, leading to decreased microbial community stability. Non-targeted metabolomic analysis identified a variety of differential metabolites, primarily associated with arginine and histidine biosynthesis. A significant increase in glutamate levels was also observed in the hippocampus of FP chickens. Transcriptome analysis revealed the upregulated expressions of glutamate-related receptors <i>GRIN2A</i> and <i>SLC17A6</i> in the hippocampus. Correlation analysis indicated that <i>GRIN2A</i> and <i>SLC17A6</i> are positively associated with arginine levels in the duodenum, while <i>Romboutsia</i> in the duodenum is negatively correlated with arginine. These findings suggest that intestinal bacteria, including <i>Romboutsia</i>, may influence FP behavior by altering plasma arginine and histidine levels. These changes, in turn, affect glutamate levels and receptor gene expression in the hippocampus, thereby regulating the glutamatergic system. Our research offers insights into novel strategies for mitigating harmful behaviors in poultry farming, with potential benefits for animal performance and welfare.
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spelling doaj-art-476e2f7653024f019174ed5d6434d3f12025-08-20T02:58:43ZengMDPI AGAnimals2076-26152025-04-01159129710.3390/ani15091297The Glutamatergic System Regulates Feather Pecking Behaviors in Laying Hens Through the Gut–Brain AxisXiliang Yan0Chao Wang1Yaling Li2Yating Lin3Yinbao Wu4Yan Wang5Heyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaHeyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaHeyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaHeyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaHeyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaHeyuan Branch, Guangdong Laboratory for Lingnan Modern Agriculture, College of Animal Science, South China Agricultural University, Guangzhou 510642, ChinaFeather pecking (FP) is a significant welfare and economic problem in laying hen husbandry. While there is growing evidence that the glutamatergic system plays a crucial role in regulating FP behavior, the biological mechanisms remain unclear, largely due to the limited uptake of peripheral glutamate across the blood–brain barrier (BBB). Here, we applied a multi-omics approach combined with physiology assays to answer this question from the perspective of the gut–brain axis. A total of 108 hens were randomly assigned to two groups (treatment and control) with six replicates each, and the treatment group was subjected to chronic environmental stressors including re-housing, noise, and transport. We found that chronic exposure to environmental stressors induced severe FP, accompanied by reduced production performance and increased anxiety- and depression-related behaviors, compared to controls. In addition, the immune system was potentially disrupted in FP chickens. Notably, gut microbiota diversity and composition were significantly altered, leading to decreased microbial community stability. Non-targeted metabolomic analysis identified a variety of differential metabolites, primarily associated with arginine and histidine biosynthesis. A significant increase in glutamate levels was also observed in the hippocampus of FP chickens. Transcriptome analysis revealed the upregulated expressions of glutamate-related receptors <i>GRIN2A</i> and <i>SLC17A6</i> in the hippocampus. Correlation analysis indicated that <i>GRIN2A</i> and <i>SLC17A6</i> are positively associated with arginine levels in the duodenum, while <i>Romboutsia</i> in the duodenum is negatively correlated with arginine. These findings suggest that intestinal bacteria, including <i>Romboutsia</i>, may influence FP behavior by altering plasma arginine and histidine levels. These changes, in turn, affect glutamate levels and receptor gene expression in the hippocampus, thereby regulating the glutamatergic system. Our research offers insights into novel strategies for mitigating harmful behaviors in poultry farming, with potential benefits for animal performance and welfare.https://www.mdpi.com/2076-2615/15/9/1297feather peckingglutamatergic systemgut–brain axisintestinal microbiotaanimal welfare
spellingShingle Xiliang Yan
Chao Wang
Yaling Li
Yating Lin
Yinbao Wu
Yan Wang
The Glutamatergic System Regulates Feather Pecking Behaviors in Laying Hens Through the Gut–Brain Axis
Animals
feather pecking
glutamatergic system
gut–brain axis
intestinal microbiota
animal welfare
title The Glutamatergic System Regulates Feather Pecking Behaviors in Laying Hens Through the Gut–Brain Axis
title_full The Glutamatergic System Regulates Feather Pecking Behaviors in Laying Hens Through the Gut–Brain Axis
title_fullStr The Glutamatergic System Regulates Feather Pecking Behaviors in Laying Hens Through the Gut–Brain Axis
title_full_unstemmed The Glutamatergic System Regulates Feather Pecking Behaviors in Laying Hens Through the Gut–Brain Axis
title_short The Glutamatergic System Regulates Feather Pecking Behaviors in Laying Hens Through the Gut–Brain Axis
title_sort glutamatergic system regulates feather pecking behaviors in laying hens through the gut brain axis
topic feather pecking
glutamatergic system
gut–brain axis
intestinal microbiota
animal welfare
url https://www.mdpi.com/2076-2615/15/9/1297
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