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

• Type of Material: Article
• Authors: Claudia Barelli, Research and Innovation Centre; Viviana Gonzalez-Astudillo, Emory University; Roger Mundry, Max-Planck Institute for Evolutionary Anthropology; Francesco Rovero, Science Museum; Heidi C. Hauffe, Research and Innovation Centre; Thomas R. Gillespie, Emory University
• Language: English
• Date: 2019-01-01
• Publisher: Public Library of Science
• Publication Version: Final Published Version
• Copyright Statement: © 2019 Barelli et al.
• License: Creative Commons Attribution 4.0 International
• Final Published Version (URL): http://dx.doi.org/10.1371/journal.pone.0225142
• Title of Journal or Parent Work: PLoS ONE
• ISSN: 1932-6203
• Volume: 14
• Issue: 12
• Start Page: e0225142
• End Page: e0225142
• Grant/Funding Information: Data collection and analyses were funded by the Provincia Autonoma di Trento and the EU (Marie Curie Actions TRENTINO COFUND); the Rufford Small Grants Foundation and the German Primate Centre (DPZ); while manuscript preparation was funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 752399.
• Research Categories: Biology, Ecology; Environmental Sciences

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.