Extensive variability in the gut microbiome of a highly-specialized and critically endangered lemur species across sites.

Deforestation continues to jeopardize Malagasy primates as viable habitats become smaller, more fragmented, and more disturbed. This deforestation can lead to changes in diet, microhabitat, and gene flow between populations of endangered species, and it remains unclear how these changes may affect gut microbiome (GM) characteristics. The black-and-white ruffed lemur (Varecia variegata), which is among Madagascar's most threatened lemur species, provides a critical model for understanding the relationships between historical and on-going deforestation (habitat disturbance), feeding ecology, and GM composition and diversity. We studied four populations inhabiting two rainforests (relatively pristine vs. highly disturbed) in southeastern Madagascar. We conducted full-day focal animal behavioral follows and collected fecal samples opportunistically across a three-month period. Our results indicate that lemurs inhabiting sites characterized by habitat disturbance and low dietary diversity exhibited reduced gut microbial alpha diversity. We also show that these same factors were associated with high community dissimilarity using weighted and unweighted UniFrac metrics. Finally, an indicator species analysis showed that the most pristine site was characterized by an abundance of methanogenic archaea. While it is impossible to disentangle the relative contributions of each confounding variable presented by our sampling design, these results provide crucial information about GM variability, thereby underscoring the importance of monitoring endangered species at the population-level.

The importance of scale in comparative microbiome research: New insights from the gut and glands of captive and wild lemurs.

Research on animal microbiomes is increasingly aimed at determining the evolutionary and ecological factors that govern host-microbiome dynamics, which are invariably intertwined and potentially synergistic. We present three empirical studies related to this topic, each of which relies on the diversity of Malagasy lemurs (representing a total of 19 species) and the comparative approach applied across scales of analysis. In Study 1, we compare gut microbial membership across 14 species in the wild to test the relative importance of host phylogeny and feeding strategy in mediating microbiome structure. Whereas host phylogeny strongly predicted community composition, the same feeding strategies shared by distant relatives did not produce convergent microbial consortia, but rather shaped microbiomes in host lineage-specific ways, particularly in folivores. In Study 2, we compare 14 species of wild and captive folivores, frugivores, and omnivores, to highlight the importance of captive populations for advancing gut microbiome research. We show that the perturbational effect of captivity is mediated by host feeding strategy and can be mitigated, in part, by modified animal management. In Study 3, we examine various scent-gland microbiomes across three species in the wild or captivity and show them to vary by host species, sex, body site, and a proxy of social status. These rare data provide support for the bacterial fermentation hypothesis in olfactory signal production and implicate steroid hormones as mediators of microbial community structure. We conclude by discussing the role of scale in comparative microbial studies, the links between feeding strategy and host-microbiome coadaptation, the underappreciated benefits of captive populations for advancing conservation research, and the need to consider the entirety of an animal's microbiota. Ultimately, these studies will help move the field from exploratory to hypothesis-driven research.

Patterns of gut bacterial colonization in three primate species.

Host fitness is impacted by trillions of bacteria in the gastrointestinal tract that facilitate development and are inextricably tied to life history. During development, microbial colonization primes the gut metabolism and physiology, thereby setting the stage for adult nutrition and health. However, the ecological rules governing microbial succession are poorly understood. In this study, we examined the relationship between host lineage, captive diet, and life stage and gut microbiota characteristics in three primate species (infraorder, Lemuriformes). Fecal samples were collected from captive lemur mothers and their infants, from birth to weaning. Microbial DNA was extracted and the v4 region of 16S rDNA was sequenced on the Illumina platform using protocols from the Earth Microbiome Project. Here, we show that colonization proceeds along different successional trajectories in developing infants from species with differing dietary regimes and ecological profiles: frugivorous (fruit-eating) Varecia variegata, generalist Lemur catta, and folivorous (leaf-eating) Propithecus coquereli. Our analyses reveal community membership and succession patterns consistent with previous studies of human infants, suggesting that lemurs may serve as a useful model of microbial ecology in the primate gut. Each lemur species exhibits distinct species-specific bacterial diversity signatures correlating to life stages and life history traits, implying that gut microbial community assembly primes developing infants at species-specific rates for their respective adult feeding strategies.

[Epidemiology of Klebsiella pneumoniae infections in 2 colonies of squirrel monkeys and lemurs]. / Epidémiologie des infections a Klebsiella pneumoniae dans deux élevages de singes-écureuils et de lémuriens.

After a short summary of the occurrence, sources, phenotypic characteristics, epidemiologic markers, virulence factors and pathogenicity of the 7 species of Klebsiella, the author reported (1) an infection due to K. pneumoniae K5 in a breed of squirrel monkey. These animals were suffering from sub-cutaneous abcesses (Pasteur Institute of Cayenne, French Guyana). (2) The second example refers a fatal infection due to K. pneumoniae K2 in a colony of lemurs, at Mulhouse zoological garden (East of France). Both animal colonies were protected against infection by the use of specific anti-K. pneumoniae capsular polysaccharide vaccine.

[Isolation of Kluyvera ascorbata from Madagascan lemurs, healthy carriers of this unusual enterobacterium]. / Isolement de Kluyvera ascorbata chez des lémuriens malgaches, porteurs sains de cette entérobactérie inhabituelle.

Six strains of Kluyvera ascorbata--an unusual species in the family Enterobacteriaceae--were isolated from six healthy lemurs, located in Tananarive's zoological garden. Their bacteriological characters are reported and compared with those of Levinea and Escherichia coli. Their occurrence and significance in animals are discussed.

Arboviruses and lemurs in Madagascar: experimental infection of Lemur fulvus with yellow fever and West Nile viruses.

In previous serological surveys of lemurs in Madagascar, antibodies against flaviviruses were frequently detected. To examine the epidemiological role of Lemur fulvus, experimental infections with yellow fever (YF) virus and West Nile (WN) virus were performed. YF and WN infections were clinically unapparent. A 3 to 4-day-long viremia, with moderate levels was observed with YF virus. WN virus, especially the strain isolated in Madagascar, provoked a 4 to 6-day-long viremia sufficient to infect Aedes aegypti. In all experiments, the antibody response was studied during the following weeks by 3 methods. The results led to the conclusion that Malagasy lemurs could act as amplifying hosts for WN virus present in Madagascar, and as hosts for YF virus if it were introduced on the island. The epidemiological role of these primates is discussed according to their ecology and their contact with potential mosquito vectors in forest areas of Madagascar.

Arboviruses and lemurs in Madagascar: a preliminary note.

The epidemiological role played by lemurs in the circulation of arboviruses in Madagascar has been studied. From serological (HAI) tests, exposure of lemurs to alphaviruses and flaviviruses appears to vary considerably with location and species of lemur; positive tests varied from 0 to 32%. Finally, the data concerning the lemurophilic part of the mosquito fauna suggests that some lemur species and man are infected by the same arboviruses, especially West Nile virus. The susceptibility of these primates to yellow fever virus, which has not yet occurred in Madagascar is under study.