Altitude and human disturbance are associated with helminth diversity in an endangered primate, Procolobus gordonorum

Abstract

Gastrointestinal parasites colonizing the mammalian gut influence the host immune system and health. Parasite infections, mainly helminths, have been studied intensively in both humans and non-human animals, but relatively rarely within a conservation framework. The Udzungwa red colobus monkey (Procolobus gordonorum) is an endangered endemic primate species living in the Udzungwa Mountains of Tanzania, a global biodiversity hotspot. Since this endemic primate species is highly sensitive to human disturbance, here we investigate whether habitat type (driven by natural and human-induced factors) is associated with helminth diversity. Using standard flotation and sedimentation techniques, we analyzed 251 fecal samples belonging to 25 social groups from four different forest blocks within the Udzungwa Mountains. Five parasitic helminth taxa were recovered from Udzungwa red colobus, including Trichuris sp., Strongyloides fulleborni, S. stercoralis, a strongylid nematode and Colobenterobius sp. We used Generalized Linear Mixed Models to explore the contribution of habitat type, altitude and fecal glucocorticoid levels (as biomarkers of stress) in predicting gut parasite variation. Although some parasites (e.g., Trichuris sp.) infected more than 50% of individuals, compared to others (e.g., Colobenterobius sp.) that infected less than 3%, both parasite richness and prevalence did not differ significantly across forests, even when controlling for seasonality. Stress hormone levels also did not predict variation in parasite richness, while altitude could explain it resulting in lower richness at lower altitudes. Because human activities causing disturbance are concentrated mainly at lower altitudes, we suggest that protection of primate forest habitat preserves natural diversity at both macro- and microscales, and that the importance of the latter should not be underestimated.

Interactions between parasitic helminths and gut microbiota in wild tropical primates from intact and fragmented habitats

“…However, they are facing escalating loss and fragmentation of optimal habitat, making this mammalian group one of the most threatened on Earth 31 . Recent research we conducted on primates living sympatrically in human-modified and pristine habitats has highlighted the impact of habitat changes on gut bacterial and fungal diversity 32 , 33 , as well as on helminth infections 34 , 35 . Although a few recent studies have evaluated the diversity and composition of the gut bacterial communities of non-human primates naturally infected by helminths 36 – 39 , here we compare both the bacterial and fungal components in helminth-positive and helminth-negative individuals to investigate: (i) whether bacterial and fungal richness and/or composition vary in primates with different ecological adaptations residing in either pristine or human-impacted forests; (ii) which bacterial and fungal taxa are responsible for such variation; and (iii) which of the detected helminths interplay with bacterial and fungal richness.…”

Red Colobus Natural History

“…They recommend establishment of corridors between the forest fragments to conserve the genetic diversity in the population. Human activities lead to smaller group sizes, while abundance is lower and parasite diversity is higher at higher elevation in the Udzungwa region (Marshall et al 2005;Barelli et al 2019). Abundance is linked to the mean basal area of large trees (>20 cm Diameter at Breast Height) and species richness of their food trees (Rovero & Struhsaker 2007).…”