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GUT biota indices: a new tool for WILD animal conservation

Periodic Reporting for period 2 - WILDGUT (GUT biota indices: a new tool for WILD animal conservation)

Periodo di rendicontazione: 2018-07-01 al 2019-06-30

Calls to stem biodiversity loss have generally focussed on the plight of charismatic vertebrates. However, although the abundance and diversity of microorganisms (including bacteria and fungi, as well as parasitic worms) inhabiting the gastrointestinal tract (‘gut biota’) have been demonstrated of critical importance to health in both humans and non-human animals, this microbiodiversity has rarely been considered within a conservation framework. While many bacteria are known to have a positive effect on our health, the combined effects of bacteria, fungi and parasitic worms has received less attention, but are likely to be essential players in gut homeostasis. Using recently collected fecal samples from two free-ranging tropical non-human primate species with contrasting ecological parameters, WILDGUT aimed at investigating wild animal gut biota in primates living in contrasting habitat types (i.e. intact versus degraded habitats) in order to identify possible biomarkers associated with conservation status that could be used to improve wildlife management strategies. Specifically, the WILDGUT project aimed to:
(i) assess the diversity and composition of gut microbiota (bacteria and fungi) and parasitic worms in two wild primate species (Udzungwa red colobus and yellow baboon) living in degraded and intact forested areas (see details about primate species and study area below);
(ii) identify potential interactions within and between microbiota and parasitic worms;
(iii) build appropriate statistical models using the dataset to identify useful indices for assessing conservation status of the primate populations;
(iv) use the results to make recommendations for animal conservation managers.
By summarizing the results obtained, we can ensure that individuals of the same primate species living in each forest type present unique gut biota compositions, especially bacteria and fungi. However, due to the different intraspecific feeding adaptation, richness per se might not be the best measure to evaluating individual health. Deeper investigations on the functional analysis of each gut component should be taken into account as well as the correlation between components. Although no particular correlations were yet detected between bacteria and fungi, the associations with parasitic worms are still on-going.
During the reporting period, the Researcher first got specific training in laboratory techniques and bioinformatics at the partner organization: the Institute for Genomic Biology (IGB), within the University of Illinois, USA. The Researcher has successfully analyzed 168 fecal samples of two wild primates living in the Udzungwa Mountains of Tanzania for bacterial, fungal and helminthes diversities and composition. Bioinformatics and statistical analyses were performed at the beneficiary host institute (FEM) where the Researcher devoted most of the time to analyzing and writing up the results obtained. Despite the fact that some analyses are still on-going, especially those referring to the interactions between biota, among the key results we achieved is the first comprehensive assessment of gut biota diversity (i.e. bacteria, fungi and parasitic worms, simultaneously) of tropical primates living in natural conditions.
Although the two selected primates are phylogenetically related, bacterial and fungal composition of their guts was clearly distinct, probably as a result of their dietary habits (e.g. red colobus are folivorous and baboons are omnivorous). That red colobus had a higher bacterial gut diversity than that of yellow baboons is also found in humans with a vegetarian vs omnivorous diets. Similarly, leaf-eating red colobus monkeys presented higher fungal richness than the omnivorous baboons, consistent with previous findings indicating that hosts with high gut fungal richness might be more efficient in breaking down plant fibers.
In addition, despite the short geographical distance separating the intact and well protected forest from the degraded one, individuals of the same primate species present unique gut biota compositions in each forest type, especially bacteria and fungi. However, although intact habitats are expected to offer their animal inhabitants a more diverse diet, the WILDGUT results support this hypothesis only for the arboreal and strictly leaf-eating red colobus monkey. We did not find the same association within the omnivorous, crop-raiding baboon. We conclude that due to the rapid conversion of tropical forest in agricultural croplands, baboons living in proximity to human settlements have altered their behavioural strategies by feeding on human food waste and cultivations. By widening their dietary choices, baboons most likely increased their bacterial richness and consequently changed their gut biota composition. However, this increase may not be entirely positive; for example, we observed that baboons living in degraded habitats had an enrichment of bacterial genera such as Sarcina and Prevotella which are generally associated with consumption of sugar-rich food and potentially linked to chronic gut inflammatory conditions and implicated in gut diseases.
Also for parasitic worms, another important component of the gut, we found a reduction of parasite diversity in animals living the degraded forests compared to those from intact forests. This result confirms those found for bacteria, and strengthens the idea that habitat changes also promote biodiversity loss at a micro scale. Thus, the need for further investigations on the health impacts of changes in the different components of the gut biota and their interactions on conservation is ever more urgent.
Since gut biota diversity is of primary importance for host health, if depletion of one of the components (e.g. bacteria, fungi and parasitic worms) occurs, plausibly also functional metagenome variation may occur, resulting in a less adaptable host, more vulnerable to abrupt changes and to pathogen invasions. Thus, gut biota could be used as a tool for assessing individual health, particularly for threatened taxa for which only non-invasive samples like fecal pellets are available. Despite the WILDGUT project did not apply any new technologies, we applied those already available within new contexts. For example, we used machine learning models (applied increasingly in medicine and healthcare) to investigate whether gut microbiota composition is associated with habitat of origin. Our analysis showed that almost all samples were correctly assigned to the forest where they were collected on the basis of their bacterial and fungal compositions. This means that the gut microbiota of each Udzungwa primate population provides a distinctive signature of the forested area from which it belongs, and this signature could potentially be used as a biomarker of their habitat of origin. Thus, if the gut biota can serve as reliable biomarker, monitoring changes in this composition could indicate changes in habitat and/or individual health and species conservation status. The project aimed at reaching conservation agencies, stakeholders, administrative and executive local authorities for the conservation and management of non-human primates and other endangered species, based on the potential use of micro-biodiversity indices as predictive tools for determining animal conservation status.
Three individuals of yellow baboons from the Udzungwa Mountains of Tanzania.
Endangered and endemic Udzungwa red colobus monkey from the Udzungwa Mountains of Tanzania.