Disentangling the Possible Drivers of Indri indri Microbiome: A Threatened Lemur Species of Madagascar

Research on the gut microbiome may help with increasing our understanding of primate health with species’ ecology, evolution, and behavior. In particular, microbiome-related information has the potential to clarify ecology issues, providing knowledge in support of wild primates conservation and their associated habitats. Indri (Indri indri) is the largest extant living lemur of Madagascar. This species is classified as “critically endangered” by the IUCN Red List of Threatened Species, representing one of the world’s 25 most endangered primates. Indris diet is mainly folivorous, but these primates frequently and voluntarily engage in geophagy. Indris have never been successfully bred under human care, suggesting that some behavioral and/or ecological factors are still not considered from the ex situ conservation protocols. Here, we explored gut microbiome composition of 18 indris belonging to 5 different family groups. The most represented phyla were Proteobacteria 40.1 ± 9.5%, Bacteroidetes 28.7 ± 2.8%, Synergistetes 16.7 ± 4.5%, and Firmicutes 11.1 ± 1.9%. Further, our results revealed that bacterial alpha and beta diversity were influenced by indri family group and sex. In addition, we investigated the chemical composition of geophagic soil to explore the possible ecological value of soil as a nutrient supply. The quite acidic pH and high levels of secondary oxide-hydroxides of the soils could play a role in the folivorous diet’s gut detoxification activity. In addition, the high contents of iron and manganese found the soils could act as micronutrients in the indris’ diet. Nevertheless, the concentration of a few elements (i.e., calcium, sulfur, boron, nickel, sodium, and chromium) was higher in non-geophagic than in geophagic soils. In conclusion, the data presented herein provide a baseline for outlining some possible drivers responsible for the gut microbiome diversity in indris, thus laying the foundations for developing further strategies involved in indris’ conservation

I Like the Way You Eat It: Lemur (Indri indri) Gut Mycobiome and Geophagy

Here, we investigated the possible linkages among geophagy, soil characteristics, and gut mycobiome of indri (Indri indri), an endangered lemur species able to survive only in wild conditions. The soil eaten by indri resulted in enriched secondary oxide-hydroxides and clays, together with a high concentration of specific essential micronutrients. This could partially explain the role of the soil in detoxification and as a nutrient supply. Besides, we found that soil subject to geophagy and indris’ faeces shared about 8.9% of the fungal OTUs. Also, several genera (e.g. Fusarium, Aspergillus and Penicillium) commonly associated with soil and plant material were found in both geophagic soil and indri samples. On the contrary, some taxa with pathogenic potentials, such as Cryptococcus, were only found in indri samples. Further, many saprotrophs and plant-associated fungal taxa were detected in the indri faeces. These fungal species may be involved in the digestion processes of leaves and could have a beneficial role in their health. In conclusion, we found an intimate connection between gut mycobiome and soil, highlighting, once again, the potential consequent impacts on the wider habitat. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00248-020-01677-5

Influences des Pressions Anthropiques sur les Lémuriens d’Anantaka, dans la Partie Est du Plateau de Makira, Maroantsetra, Madagascar

L’équipe de Groupe d’Etude et de Recherche sur les Primates de Madagascar (GERP), pour contribuer dans la protection, a prospecté et suivi 12 sites dans la forêt de Makira dont Anantaka pendant les mois de septembre et octobre 2005 et 2006. A l’aide des lignes - inventaire, la densité relative de la population de lémuriens a été obtenue par des observations directes tandis que les pressions humaines ont été inventoriées par l‘évaluation des surfaces d‘incidence des activités humaines. Des activités anthropiques sur les lémuriens ont été identifiées. Les influences de chaque type de pression sur les espèces de Lémuriens (trois diurnes strictes, une cathémérale et dix nocturnes) répertoriées à travers 12 sites ont été analysées à partir du coefficient de corrélation R de Spearman entre chaque facteur menaçant par rapport à chaque effectif de lémurien. Ainsi, d’une part, on a déduit que le site d’Anantaka, avec ses 14 espèces lémuriennes, est le plus riche en espèces de lémuriens. Et d’autre part, on a constaté que plus le nombre de village est abondant et plus leur distance par rapport à la forêt est rapprochée et que les impacts de pression sur l’écosystème forestier augmente avec des activités relatives comme la chasse, les coupes illicites, les défrichements de la forêt primaire, les défrichements des forêts secondaires et la transformation des forêts en tavy ou en kijana (prairie) ainsi que les exploitations minières illicites. A part cette dégradation de la biodiversité, la décadence de la moralité à la fois sur les notions du civisme et le concept du fady (tabou) en l’encontre des Aye aye par exemple, se trouve sur une situation bouleversante, puisque les gens ne considèrent plus ni les valeurs culturelles pour la conservation de la forêt ni les lois régissant la gestion forestière et les chasses des animaux sauvages. Ces critères classifient le site d’Anantaka dans la cible focale de conservation du fait que la couverture forestière d’Anantaka présente encore 75% de forêt, 25% est transformée en savoka et en prairie. C’est ainsi que l’indispensablement d’une priorité en matière de conservation des lémuriens pour conserver la niche écologique exceptionnelle d’Anantaka. La conservation de Makira serait optimale avec l’intégration de la population riveraine du site d’Anantaka dans la gestion rationnelle de leurs ressources naturelles et avec l’intervention de l’éducation environnementale dans quelques localités dont les Communautés de base (COBA) et avec l’appui technique émanant des associations dans l’élaboration d’un plan de développement touchant surtout l’agriculture et d’un projet qui assurera la surveillance et le contrôle du secteur par des missions de suivi - évaluation

I Like the Way You Eat It: the possible environmental drivers of Lemur (Indri indri) Gut Microbiome and Mycobiome

Research on gut microbiome may help with increasing our understanding of primate health with species\u2019 ecology, evolution, and behavior. Microbiome-related information has the potential to clarify ecology issues, providing knowledge in support of wild primates\u2019 conservation and their associated habitats. Indri (Indri indri) is the largest extant living lemur of Madagascar able to survive only in wild conditions. This species is classified as \u201ccritically endangered\u201d by the IUCN Red List of Threatened Species, representing one of the world\u2019s 25 most endangered primates. Indris diet is mainly folivorous, but these primates frequently and voluntarily engage in geophagy. Here, we investigated the possible linkages among geophagy, soil characteristics, and gut microbiome and mycobiome of indri (Indri indri). In these works, we explored the chemical composition of soil eaten by indri, which resulted rich in secondary oxide-hydroxides and clays, together with a high concentration of specific essential micronutrients. This could partially explain the role of the soil in detoxification and as a nutrient supply. Then, we explored the gut microbiome composition of 18 indris belonging to 5 different family groups. The most represented phyla were Proteobacteria 40.1 \ub1 9.5%, Bacteroidetes 28.7 \ub1 2.8%, and Synergistetes 16.7 \ub1 4.5%. Besides, we found that soil subject to geophagy and indris\u2019 faeces shared about 8.9% of the fungal OTUs. Also, several genera (e.g. Fusarium, Aspergillus and Penicillium) were found in both geophagic soil and indri samples. In conclusion, the intimate connection between gut mycobiome and soil, demonstrated that fungal species may be involved in the digestion processes of leaves and could have a beneficial role in their health. Altogether, the data presented in our works, provide a baseline for outlining some possible drivers responsible for the gut microbiome and mycobiome diversity in indris, thus laying the foundations for developing further strategies involved in indris\u2019 conservation