The twenty-first century has witnessed a wave of severe infectious disease outbreaks, not least the COVID-19 pandemic, which has had a devastating impact on lives and livelihoods around the globe. The 2003 severe acute respiratory syndrome coronavirus outbreak, the 2009 swine flu pandemic, the 2012 Middle East respiratory syndrome coronavirus outbreak, the 2013–2016 Ebola virus disease epidemic in West Africa and the 2015 Zika virus disease epidemic all resulted in substantial morbidity and mortality while spreading across borders to infect people in multiple countries. At the same time, the past few decades have ushered in an unprecedented era of technological, demographic and climatic change: airline flights have doubled since 2000, since 2007 more people live in urban areas than rural areas, population numbers continue to climb and climate change presents an escalating threat to society. In this Review, we consider the extent to which these recent global changes have increased the risk of infectious disease outbreaks, even as improved sanitation and access to health care have resulted in considerable progress worldwide.

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As human population density continues to increase exponentially, speeding the reduction and fragmentation of primate habitat, greater human-primate contact is inevitable, making higher rates of pathogen transmission likely. Anthropogenic effects are particularly evident in Madagascar, where a diversity of endemic lemur species are threatened by rapid habitat loss. Despite these risks, knowledge of how anthropogenic activities affect lemur exposure to pathogens is limited. To improve our understanding of this interplay, we non-invasively examined six species of wild lemurs in Ranomafana National Park for enteric bacterial pathogens commonly associated with diarrheal disease in human populations in Madagascar. Patterns of infection with Enterotoxigenic Escherichia coli, Shigella spp., Salmonella enterica, Vibrio cholerae, and Yersinia spp. (enterocolitica and pseudotuberculosis) were compared between lemurs inhabiting intact forest and lemurs inhabiting degraded habitat with frequent exposure to tourism and other human activity. Fecal samples acquired from humans, livestock, and rodents living near the degraded habitat were also screened for these bacteria. Remarkably, only lemurs living in disturbed areas of the park tested positive for these pathogens. Moreover, all of these pathogens were present in the human, livestock, and/or rodent populations. These data suggest that lemurs residing in forests altered or frequented by people, livestock, or peridomestic rodents, are at risk for infection by these diarrhea-causing enterobacteria and other similarly transmitted pathogens.

Health and nutritional assessments of wildlife are important management tools and can provide a means to evaluate ecosystem health. Such examinations were performed on 37 white-fronted brown lemurs (Eulemur fulvus albifrons) from four sites in Madagascar. Comparison of health parameters between sites revealed statistically significant differences in body weight, body temperature, respiratory rate, hematology parameters (white cell count, hematocrit, segmented neutrophil count, and lymphocyte count), serum chemistry parameters (aspartate aminotransferase, alanine aminotransferase, serum alkaline phosphatase, total protein, albumin, phosphorus, calcium, sodium, chloride, and creatinine phosphokinase), and nutrition parameters (copper, zinc, ferritin, retinol, tocopherol, and 25-hydroxycholecalciferol). Two of 10 lemurs tested were positive for toxoplasmosis; none of 10 were positive for Cryptosporidium or Giardia. Enteric bacteria and endo- and ectoparasites were typical. Statistically different values in hematology and chemistry values probably do not reflect clinically significant differences, whereas nutrition parameter differences are likely related to season, soil, and forage availability.

BackgroundAmong the families of enteric bacteria are globally important diarrheal agents. Despite their potential for zoonotic and environmental transmission, few studies have examined the epidemiology of these pathogens in rural systems characterized by extensive overlap among humans, domesticated and peridomestic animals. We investigated patterns of infection with Enterotoxigenic Escherichia coli, Shigella spp., Salmonella enterica, Vibrio cholerae, and Yersinia spp. (enterocolitica, and pseudotuberculosis) in Southeastern Madagascar where the potential for the aforementioned interactions is high. In this pilot project we conducted surveys to examine behaviors potentially associated with risk of infection and if infection with specific enterobacteria species was associated with diarrheal disease.Methodology/Principal FindingsPCR was conducted on DNA from human, livestock, and rodent fecal samples from three villages. Overall, human prevalence was highest (77%), followed by rodents (51%) and livestock (18%). Rodents were ∼2.8 times more likely than livestock to carry one of the bacteria. The incidence of individual species varied between villages, with the observation that, E. coli and Shigella spp. were consistently associated with co-infections. As an aggregate, there was a significant risk of infection linked to a water source in one village. Individually, different pathogens were associated with certain behaviors, including: those who had used medication, experienced diarrhea in the past four weeks, or do not use toilets.Conclusions/SignificanceDifferent bacteria were associated with an elevated risk of infection for various human activities or characteristics. Certain bacteria may also predispose people to co-infections. These data suggest that a high potential for transmission among these groups, either directly or via contaminated water sources. As these bacteria were most prevalent in humans, it is possible that they are maintained in humans and that transmission to other species is infrequent. Further studies are needed to understand bacterial persistence, transmission dynamics, and associated consequences in this and similar systems.

Madagascar is a biodiversity hotspot that is facing rapid rates of deforestation, habitat destruction, and poverty. Urgent action is required to document the status of biodiversity to facilitate efficacious conservation plans. With the recent advent of portable and affordable genetic technologies, it is now possible to take genomic approaches out of the lab and into the field. Mobile genetics labs can produce scientifically reproducible data under field conditions, dramatically minimizing the time between sample collection and data analysis. Here, we show “proof of concept” by deploying miniPCR bio’s miniaturized thermal cycler alongside Oxford Nanopore’s MinION DNA sequencer in Madagascar. Specifically, we deployed this technology at Anjajavy, northwestern Madagascar for rapid biodiversity assessment. We successfully extracted mouse lemur DNA, amplified and sequenced a phylogenetically informative mitochondrial gene (cytochrome-b; cytb), and thereby confirmed the presence of Danfoss’ mouse lemur (M. danfossi) within the Anjajavy Reserve. We show that a mobile genetics lab can provide expeditious results, and allow scientists to conduct genetic analyses, potentially allowing for rapid interventions under emergency conditions in situ. Additionally, mobile labs offer powerful training opportunities for in-country scientists for whom training opportunities were previously confined to ex-situ locations. By bringing genomic technologies to Madagascar and other economically challenged and biodiverse regions of the world, the next generation of scientists and conservationists can more fully implement their leadership roles. Local laboratory and training facilities are changing the polarity of research programs in Madagascar and empowering national researchers to take charge of environmental stewardship.

Introduced carnivores exert considerable pressure on native predators through predation, competition and disease transmission. Recent research shows that exotic carnivores negatively affect the distribution and abundance of the native and endangered carnivores of Madagascar. In this study, we provide information about the frequency and distribution of interactions between exotic (dogs and cats) and native carnivores (Eupleridae) in the Betampona Natural Reserve (BNR), Madagascar, using noninvasive camera trap surveys. Domestic dogs (Canis familiaris) were the most frequently detected carnivore species within the BNR, and we found that indirect interactions between exotic and native carnivores were frequent (n = 236). Indirect interactions were more likely to occur near the research station (incidence rate ratio = 0.91), which may constitute a disease transmission hot spot for carnivores at BNR. The intervals between capture of native and exotic carnivores suggest that there is potential for pathogen transmission between species in BNR. These capture intervals were significantly shorter near the edge of the reserve (P = 0.04). These data could be used to implement biosecurity measures to monitor interactions and prevent disease transmission between species at the domestic animal and wildlife interface.