The relationship between pinworm (Trypanoxyuris) infection and gut bacteria in wild black howler monkeys (Alouatta pigra)

Abstract

Gut bacteria may coexist with other groups of organisms, such as nematode parasites, that inhabit the gastrointestinal tract of primates; however, the possible effects of endoparasites on bacterial communities are frequently overlooked. Here we explored whether infection with Trypanoxyuris, an oxyurid gastrointestinal parasite, is associated with changes in the gut bacterial community of wild black howler monkeys (Alouatta pigra), by comparing gut bacterial communities of consistently infected individuals and individuals that never tested positive for Trypanoxyuris throughout different months across the year. We additionally controlled for other sources of variation reported to influence the primate microbiome including individual identity, social group, and seasonality. Trypanoxyuris infection was not related to differences in gut bacterial alpha diversity, but was weakly associated with differences in gut bacterial community structure. In contrast, among the covariates considered, both individual identity and social group were more strongly associated with variation in the howler gut bacterial community. Our results suggest that gastrointestinal parasites may be associated, to some extent, with shifts in the gut bacterial communities hosted by free-ranging primates, although a causal link still needs to be established. Further studies of wild primate hosts infected with parasite species with different pathogenicity are needed to better elucidate health-related consequences from the parasite-microbiome interplay.

Assessing the drivers of gut microbiome composition in wild redfronted lemurs via longitudinal metacommunity analysis

“…Our results support previous reports from redfronted lemurs that detected seasonal differences in the abundances of Chromadorea , and protozoa diversity 73 . Parasite richness only explained very low variation in bacterial beta diversity but associated positively and also negatively with certain bacterial taxa, supporting other studies from non-human primates 28 – 30 . Positive associations with Succinivibrio and Verrucomicrobiota have been reported in humans as well 74 , 75 .…”

“…For instance, in non-human primates, higher bacterial alpha diversity correlates to higher eukaryotic diversity 27 . Therefore, the presence of helminths and/or protozoa may impact the abundances of bacterial taxa [28][29][30] . Despite being challenging, research on wild animals provide an exceptional possibility to apply metacommunity concepts for investigating the drivers of the gut microbiome in undisturbed scenarios 5,8 .…”

Gastrointestinal symbiont diversity in wild gorilla: A comparison of bacterial and strongylid communities across multiple localities

“…Helminth infection has partially explained bacterial microbiome variation in wild lemurs, though findings were not consistent when the studied populations were analysed separately (de Winter et al, 2020). In wild black howler monkeys ( Alouatta pigra ), differences in the community composition of gut bacteria were weakly associated with pinworm ( Trypanoxyuris ) infection, a gastrointestinal helminth, though a better understanding of the parasite–microbiome interplay was called for (Martínez‐Mota et al, 2021).…”

Environmental Stress and the Primate Microbiome: Glucocorticoids Contribute to Structure Gut Bacterial Communities of Black Howler Monkeys in Anthropogenically Disturbed Forest Fragments

“…It will also be important to explore the extent to which the magnitude of these effects varies across different host species and the physiological pathways that contribute to this variation. Although several populations of black howler monkeys inhabit highly disturbed tropical forests (Pozo-Montuy et al, 2011;Rangel-Negrín et al, 2014b;Klass et al, 2020;Martínez-Mota et al, 2021) and are most likely exposed to environmental stressors (Martínez-Mota et al, 2007;Behie and Pavelka, 2013;Rangel-Negrín et al, 2014a), these primates might have coping mechanisms to deal with food availability deficits resulting from forest loss and fragmentation. For instance, found that SCFA produced by gut bacteria of howler monkeys were increased during periods of low energy intake, which suggests that microbial metabolism may support energy availability under critical periods of low food intake.…”