How does anthropogenic impact affect the microbiome of Howler monkeys (genus Alouatta) in Bolivia?

By Maxime Mees, 2025
MS Thesis, Université libre de Bruxelles (ULB, Belgium)
In collaboration with the Noel Kempff Mercado Natural History Museum (UAGRM)

A summary for non-specialists

Human activities increasingly shape the environments in which wildlife lives, both directly through captivity and indirectly through habitat modification. In Bolivia, howler monkeys of the genus Alouatta occur in a wide range of natural and human-influenced settings, including forests, botanical gardens, rescue centers, and zoos.

While the visible effects of captivity and human contact on animal behavior are well recognized, less is known about how these conditions influence internal biological systems such as the gut microbiome, which plays a key role in digestion, immunity, and overall health.

The objective of this study was to evaluate how anthropogenic environments affect the gut microbiome of Bolivian howler monkeys, focusing on two species: Alouatta sara and Alouatta caraya.

To address this question, fecal samples were collected using a non-invasive approach from individuals living in natural environments (free-ranging populations) and from individuals living in anthropogenic environments such as zoological institutions and wildlife rescue centers. This allowed direct comparison between animals exposed to minimal human influence and those living under managed or captive conditions.

Natural sampling sites included forested areas where one or both species occur. Anthropogenic sites included rescue centers and a municipal zoo, where animals are exposed to managed diets, veterinary care, supplements, and frequent human contact. Fecal samples were also used to genetically confirm species identity.

The results indicate that anthropogenic environments do not necessarily reduce overall gut bacterial diversity. In other words, captive monkeys do not appear to host fewer bacterial species than wild individuals.

However, while diversity levels remain similar, the composition of the microbiome differs significantly between environments.

In natural habitats, the microbiome includes bacteria associated with plant digestion, forest ecosystems, and natural food sources.

In contrast, monkeys in anthropogenic environments show microbiomes influenced by human-associated bacteria, managed diets, and probiotic-related microorganisms.

Many bacteria commonly used as probiotics in humans and domestic animals were found in higher abundance in captive individuals. These may be introduced intentionally through supplements or unintentionally via human contact, food preparation, or veterinary care.

These findings show that human influence reshapes the microbiome rather than reducing it. Natural microbial communities may be partially replaced by bacteria linked to anthropogenic conditions.

Importantly, this shift is driven mainly by habitat type (natural vs anthropogenic), while differences between species play a secondary role.

Conservation implications: The gut microbiome is crucial for digestion efficiency, immune function, and disease resistance. Changes in microbiome composition may affect long-term health, especially for animals intended for reintroduction into the wild.

Broader significance: This study provides a non-invasive methodology applicable to other primates, opens the door to long-term microbiome studies, and supports the integration of microbiome science into conservation strategies.

Future research could explore expanded sampling, long-term changes, and the role of hybridization between Alouatta sara and Alouatta caraya.

Conclusion: Human influence significantly alters the composition of the gut microbiome in Bolivian howler monkeys, even when overall diversity remains stable. These findings highlight the importance of considering microbial health in wildlife management and conservation.

---

¿Cómo afecta el impacto antropogénico al microbioma intestinal de monos aulladores (género Alouatta) en Bolivia?

Maxime Mees, 2025
Tesis de Maestría, Université libre de Bruxelles (Bélgica)
En colaboración con el Museo de Historia Natural Noel Kempff Mercado (UAGRM)

Resumen para no especialistas

Las actividades humanas influyen cada vez más en los entornos donde habita la fauna silvestre, tanto directamente a través del cautiverio como indirectamente mediante la modificación del hábitat.

En Bolivia, los monos aulladores del género Alouatta viven en distintos ambientes, desde bosques naturales hasta zoológicos, jardines botánicos y centros de rescate.

Aunque los efectos visibles del cautiverio son bien conocidos, se sabe menos sobre cómo estas condiciones afectan sistemas internos como el microbioma intestinal, clave para la digestión, la inmunidad y la salud general.

El estudio evaluó cómo estos entornos afectan el microbioma intestinal de los monos aulladores, centrándose en Alouatta sara y Alouatta caraya.

Se recolectaron muestras fecales de manera no invasiva tanto de poblaciones silvestres como de individuos en cautiverio, permitiendo una comparación directa.

Los resultados muestran que la diversidad bacteriana no necesariamente disminuye en ambientes antropogénicos, pero la composición del microbioma sí cambia significativamente.

En ambientes naturales predominan bacterias asociadas a la digestión de plantas y ecosistemas forestales.

En ambientes antropogénicos aparecen bacterias asociadas a humanos, dietas controladas y microorganismos relacionados con probióticos.

Esto indica que la influencia humana transforma el microbioma.

Estos cambios pueden afectar la salud, la adaptación y el éxito de reintroducción en la naturaleza.

Un microbioma adaptado a condiciones humanas puede no ser adecuado para la vida silvestre.

El estudio resalta la importancia de integrar el análisis del microbioma en estrategias de conservación y manejo de fauna silvestre.

Conclusión: La influencia humana altera significativamente la composición del microbioma intestinal de los monos aulladores, incluso cuando la diversidad se mantiene.