Background <p>Colobine monkey species have a multi-cavity forestomach adapted to a folivorous diet and foregut fermentation, making their gut microbiome essential for efficient digestion of plant fibre. In captivity, these species frequently experience gastrointestinal disorders associated with dietary changes and microbial dysbiosis. Understanding how their microbiome differs from that of other primates is therefore critical for improving health and husbandry. This study used a meta-analysis of global primate microbiome data to compare the faecal microbiome of colobines with those of other herbivorous primates, focusing on the effects of captivity.</p> Results <p>Data from 16 studies involving 35 primate species and 7 primate families/subfamilies, comprising 1,690 faecal samples generated using 16&#xa0;S rRNA amplicon sequencing, were re-analysed using standardised bioinformatic and compositional-statistical pipelines. Significant differences in microbial diversity and composition were observed among wild primates across families/subfamilies, diets, and fermentation strategies. Colobinae had a distinctive microbiome characterised by low Shannon diversity and high relative abundance of Firmicutes, particularly Ruminococcaceae and Lachnospiraceae, which were also prominent members of the wild colobinae core microbiome. Across all families/subfamilies and within colobinae, observed Shannon diversity was lower in captivity; however, multivariable mixed-effects models showed that alpha-diversity estimates were highly sensitive to study identity, species representation and methodological covariates. In contrast, beta-diversity and ALDEx2 analyses provided consistent evidence of captivity-associated compositional restructuring. Captive colobinae were enriched in Bacteroidetes and Spirochaetes, and families such as Prevotellaceae, Rikenellaceae, Methanobacteriaceae, Spirochaetaceae and Bacteroidaceae, whereas wild colobines were enriched in fibre-associated taxa, including Ruminococcaceae and Lachnospiraceae.</p> Conclusions <p>Captivity alters the gut microbiota of colobine primates, affecting microbial diversity and core fibre-fermenting taxa important for gastrointestinal health. However, adjusted alpha-diversity models revealed substantial confounding by study, species, and methodological variables, indicating that diversity effects should be interpreted cautiously. Their specialised folivorous diet and foregut-fermenting physiology appear to produce a highly efficient yet fragile microbial ecosystem poorly adapted to ex-situ conditions. The strongest evidence for captivity-associated disruption was consistent alterations in faecal microbial composition, highlighting the need for diet formulations and microbiome-based health monitoring tailored to the unique digestive ecology of colobines to mitigate the high prevalence of gastrointestinal disorders in captivity.</p>

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Colobine gut microbiome vulnerability to captivity: a meta-analysis of herbivorous primates

  • Marta Todó-Llorens,
  • Nicola Rooney,
  • Laura Peachey

摘要

Background

Colobine monkey species have a multi-cavity forestomach adapted to a folivorous diet and foregut fermentation, making their gut microbiome essential for efficient digestion of plant fibre. In captivity, these species frequently experience gastrointestinal disorders associated with dietary changes and microbial dysbiosis. Understanding how their microbiome differs from that of other primates is therefore critical for improving health and husbandry. This study used a meta-analysis of global primate microbiome data to compare the faecal microbiome of colobines with those of other herbivorous primates, focusing on the effects of captivity.

Results

Data from 16 studies involving 35 primate species and 7 primate families/subfamilies, comprising 1,690 faecal samples generated using 16 S rRNA amplicon sequencing, were re-analysed using standardised bioinformatic and compositional-statistical pipelines. Significant differences in microbial diversity and composition were observed among wild primates across families/subfamilies, diets, and fermentation strategies. Colobinae had a distinctive microbiome characterised by low Shannon diversity and high relative abundance of Firmicutes, particularly Ruminococcaceae and Lachnospiraceae, which were also prominent members of the wild colobinae core microbiome. Across all families/subfamilies and within colobinae, observed Shannon diversity was lower in captivity; however, multivariable mixed-effects models showed that alpha-diversity estimates were highly sensitive to study identity, species representation and methodological covariates. In contrast, beta-diversity and ALDEx2 analyses provided consistent evidence of captivity-associated compositional restructuring. Captive colobinae were enriched in Bacteroidetes and Spirochaetes, and families such as Prevotellaceae, Rikenellaceae, Methanobacteriaceae, Spirochaetaceae and Bacteroidaceae, whereas wild colobines were enriched in fibre-associated taxa, including Ruminococcaceae and Lachnospiraceae.

Conclusions

Captivity alters the gut microbiota of colobine primates, affecting microbial diversity and core fibre-fermenting taxa important for gastrointestinal health. However, adjusted alpha-diversity models revealed substantial confounding by study, species, and methodological variables, indicating that diversity effects should be interpreted cautiously. Their specialised folivorous diet and foregut-fermenting physiology appear to produce a highly efficient yet fragile microbial ecosystem poorly adapted to ex-situ conditions. The strongest evidence for captivity-associated disruption was consistent alterations in faecal microbial composition, highlighting the need for diet formulations and microbiome-based health monitoring tailored to the unique digestive ecology of colobines to mitigate the high prevalence of gastrointestinal disorders in captivity.