@article{bornbusch_greene_rahobilalaina_calkins_rothman_clarke_lafleur_drea_2022, title={Gut microbiota of ring-tailed lemurs (Lemur catta) vary across natural and captive populations and correlate with environmental microbiota}, volume={4}, ISSN={["2524-4671"]}, DOI={10.1186/s42523-022-00176-x}, abstractNote={Abstract
                Background
                Inter-population variation in host-associated microbiota reflects differences in the hosts’ environments, but this characterization is typically based on studies comparing few populations. The diversity of natural habitats and captivity conditions occupied by any given host species has not been captured in these comparisons. Moreover, intraspecific variation in gut microbiota, generally attributed to diet, may also stem from differential acquisition of environmental microbes—an understudied mechanism by which host microbiomes are directly shaped by environmental microbes. To more comprehensively characterize gut microbiota in an ecologically flexible host, the ring-tailed lemur (Lemur catta; n = 209), while also investigating the role of environmental acquisition, we used 16S rRNA sequencing of lemur gut and soil microbiota sampled from up to 13 settings, eight in the wilderness of Madagascar and five in captivity in Madagascar or the U.S. Based on matched fecal and soil samples, we used microbial source tracking to examine covariation between the two types of consortia.
              
                Results
                The diversity of lemur gut microbes varied markedly within and between settings. Microbial diversity was not consistently greater in wild than in captive lemurs, indicating that this metric is not necessarily an indicator of host habitat or environmental condition. Variation in microbial composition was inconsistent both with a single, representative gut community for wild conspecifics and with a universal ‘signal of captivity’ that homogenizes the gut consortia of captive animals. Despite the similar, commercial diets of captive lemurs on both continents, lemur gut microbiomes within Madagascar were compositionally most similar, suggesting that non-dietary factors govern some of the variability. In particular, soil microbial communities varied across geographic locations, with the few samples from different continents being the most distinct, and there was significant and context-specific covariation between gut and soil microbiota.
              
                Conclusions
                As one of the broadest, single-species investigations of primate microbiota, our study highlights that gut consortia are sensitive to multiple scales of environmental differences. This finding begs a reevaluation of the simple ‘captive vs. wild’ dichotomy. Beyond the important implications for animal care, health, and conservation, our finding that environmental acquisition may mediate aspects of host-associated consortia further expands the framework for how host-associated and environmental microbes interact across different microbial landscapes.
              }, number={1}, journal={ANIMAL MICROBIOME}, author={Bornbusch, Sally L. and Greene, Lydia K. and Rahobilalaina, Sylvia and Calkins, Samantha and Rothman, Ryan S. and Clarke, Tara A. and LaFleur, Marni and Drea, Christine M.}, year={2022}, month={Apr} }
 @article{bornbusch_clarke_hobilalaina_reseva_lafleur_drea_2022, title={Microbial rewilding in the gut microbiomes of captive ring-tailed lemurs (Lemur catta) in Madagascar}, volume={12}, ISSN={["2045-2322"]}, DOI={10.1038/s41598-022-26861-0}, abstractNote={AbstractMicrobial rewilding, whereby exposure to naturalistic environments can modulate or augment gut microbiomes and improve host-microbe symbiosis, is being harnessed as an innovative approach to human health, one that may also have significant value to animal care and conservation. To test for microbial rewilding in animal microbiomes, we used a unique population of wild-born ring-tailed lemurs (Lemur catta) that were initially held as illegal pets in unnatural settings and, subsequently, relocated to a rescue center in Madagascar where they live in naturalistic environments. Using amplicon and shotgun metagenomic sequencing of lemur and environmental microbiomes, we found multiple lines of evidence for microbial rewilding in lemurs that were transitioned from unnatural to naturalistic environments: A lemur’s duration of exposure to naturalistic settings significantly correlated with (a) increased compositional similarly to the gut communities of wild lemurs, (b) decreased proportions of antibiotic resistance genes that were likely acquired via human contact during pethood, and (c) greater covariation with soil microbiomes from natural habitats. Beyond the inherent psychosocial value of naturalistic environments, we find that actions, such as providing appropriate diets, minimizing contact with humans, and increasing exposure to natural environmental consortia, may assist in maximizing host-microbe symbiosis in animals under human care.}, number={1}, journal={SCIENTIFIC REPORTS}, author={Bornbusch, Sally L. and Clarke, Tara A. and Hobilalaina, Sylvia and Reseva, Honore Soatata and LaFleur, Marni and Drea, Christine M.}, year={2022}, month={Dec} }
 @article{filla_rajeev_randriana_hanitriniana_rafaliarison_edosoa_andriamananjara_razafindraibe_nely_ferreira_et al._2021, title={Lessons Learned and Paths Forward for Rabies Dog Vaccination in Madagascar: A Case Study of Pilot Vaccination Campaigns in Moramanga District}, volume={6}, ISSN={["2414-6366"]}, DOI={10.3390/tropicalmed6020048}, abstractNote={Canine rabies causes an estimated 60,000 human deaths per year, but these deaths are preventable through post-exposure prophylaxis of people and vaccination of domestic dogs. Dog vaccination campaigns targeting 70% of the population are effective at interrupting transmission. Here, we report on lessons learned during pilot dog vaccination campaigns in the Moramanga District of Madagascar. We compare two different vaccination strategies: a volunteer-driven effort to vaccinate dogs in two communes using static point vaccination and continuous vaccination as part of routine veterinary services. We used dog age data from the campaigns to estimate key demographic parameters and to simulate different vaccination strategies. Overall, we found that dog vaccination was feasible and that most dogs were accessible to vaccination. The static-point campaign achieved higher coverage but required more resources and had a limited geographic scope compared to the continuous delivery campaign. Our modeling results suggest that targeting puppies through community-based vaccination efforts could improve coverage. We found that mass dog vaccination is feasible and can achieve high coverage in Madagascar; however, context-specific strategies and an investment in dog vaccination as a public good will be required to move the country towards elimination.}, number={2}, journal={TROPICAL MEDICINE AND INFECTIOUS DISEASE}, author={Filla, Caitlynn and Rajeev, Malavika and Randriana, Zoavina and Hanitriniana, Chantal and Rafaliarison, Radoniaina R. and Edosoa, Glenn Torrencelli and Andriamananjara, Mamitiana and Razafindraibe, Nivohanitra P. and Nely, Jose and Ferreira, Angelique and et al.}, year={2021}, month={Jun} }
 @article{greene_clarke_southworth_bornbusch_ehmke_2020, title={Daily lettuce supplements promote foraging behavior and modify the gut microbiota in captive frugivores}, volume={39}, ISSN={["1098-2361"]}, DOI={10.1002/zoo.21555}, abstractNote={AbstractFor captive primates, greater provisioning of leafy greens or foliage can promote natural foraging behavior while boosting fiber intake. Recalcitrant fiber, although minimally available to endogenous metabolism, is readily fermented into nutrients by gut microbes. Whereas most primates in captivity consume fiber‐limited diets and harbor imbalanced gut microbiota compared to their wild conspecifics, the importance of fiber provisioning to primate gut microbiota has predominately been studied in folivores. We, therefore, determined if commercial lettuce could be used to encourage foraging behavior and modify the gut microbiota of captive frugivores. We provisioned ruffed lemurs (Varecia rubraandV. variegata) with romaine lettuce, on top of the standard dietary fare, for 10 consecutive days. Before and across the period of lettuce supplementation, we collected observational data of animal feeding and fecal samples for microbiome analysis, determined via amplicon sequencing. The ruffed lemurs and their gut microbes responded to lettuce provisioning. In particular, younger animals readily ate lettuce and showed no decline in consumption across study days. When controlling for the effects of host species and social‐group membership, lettuce consumption shifted the composition of the gut microbiome away from each lemur's own baseline, an effect that became stronger as the study progressed. In the final study days,Ruminococcaceae UCG‐008andAkkermansia, microbes typically and respectively associated with fiber metabolism and host health, were significantly enriched in the consortia of lettuce‐provisioned subjects. Ultimately, the routine offering of lettuce, leafy greens, or foliage to captive frugivores may benefit animal wellbeing.}, number={5}, journal={ZOO BIOLOGY}, author={Greene, Lydia K. and Clarke, Tara A. and Southworth, Chelsea A. and Bornbusch, Sally L. and Ehmke, Erin E.}, year={2020}, month={Sep}, pages={334–344} }
 @article{chandrashekar_knierim_khan_raboin_venkatesh_clarke_cuozzo_lafleur_lawler_parga_et al._2020, title={Genetic population structure of endangered ring-tailed lemurs (Lemur catta) from nine sites in southern Madagascar}, volume={10}, ISSN={["2045-7758"]}, DOI={10.1002/ece3.6337}, abstractNote={AbstractMadagascar's ring‐tailed lemurs (Lemur catta) are experiencing rapid population declines due to ongoing habitat loss and fragmentation, as well as increasing exploitation for bushmeat and the illegal pet trade. Despite being the focus of extensive and ongoing behavioral studies, there is comparatively little known about the genetic population structuring of the species. Here, we present the most comprehensive population genetic analysis of ring‐tailed lemurs to date from across their likely remaining geographic range. We assessed levels of genetic diversity and population genetic structure using multilocus genotypes for 106 adult individuals from nine geographically representative localities. Population structure and FST analyses revealed moderate genetic differentiation with localities being geographically partitioned into northern, southern, western and also potentially central clusters. Overall genetic diversity, in terms of allelic richness and observed heterozygosity, was high in the species (AR = 4.74, HO = 0.811). In fact, it is the highest among all published lemur estimates to date. While these results are encouraging, ring‐tailed lemurs are currently affected by ongoing habitat fragmentation and occur at lower densities in poorer quality habitats. The effects of continued isolation and fragmentation, coupled with climate‐driven environmental instability, will therefore likely impede the long‐term viability of the species.}, number={15}, journal={ECOLOGY AND EVOLUTION}, author={Chandrashekar, Aparna and Knierim, Jessica A. and Khan, Sohail and Raboin, Dominique L. and Venkatesh, Sateesh and Clarke, Tara A. and Cuozzo, Frank P. and LaFleur, Marni and Lawler, Richard R. and Parga, Joyce A. and et al.}, year={2020}, month={Aug}, pages={8030–8043} }