Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance

Abstract

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.

Impending extinction crisis of the world’s primates: Why primates matter

“…They also show an increased prevalence of parasites and pathogens. For example, the increased exposure of lemurs ( Avahi laniger , Eulemur rubriventer , Hapalemur aureus , Microcebus rufus , Propithecus edwardsi , and Prolemur simus ) and chimpanzees ( P. troglodytes ) to human populations has increased their risk of infection by diarrhea-causing enteric pathogens ( 56 , 57 ). The close phylogenetic relationship between humans and other primates also creates an exceptionally high potential for pathogen exchange ( 58 ), as evidenced by disease emergence in humans as an unintentional effect of the hunting and butchering of wild primates (for example, human outbreaks of Ebola and the global HIV/AIDS pandemic) ( 59 ).…”

Gastrointestinal Parasites of Captive and Free-Living Lemurs and Domestic Carnivores in Eastern Madagascar

“…24,35 Pathogenic enterobacteria and viruses were also found in lemurs in Ranomafana National Park. 4,48 Although parasites of domestic carnivores are known to cause disease in captive lemurs, minimal data are currently available on gastrointestinal parasites of domestic carnivores in Madagascar. 9,13,30,39,41,43,44 These data will be valuable as a baseline reference, especially as domestic animals are increasingly encroaching into Madagascar forests (Rasambainarivo, pers.…”

Blood transcriptomes reveal novel parasitic zoonoses circulating in Madagascar's lemurs

“…Moreover, they are experiencing rapid population declines owing to historical and ongoing destruction of the forests of Madagascar and the hunting of lemurs for bushmeat [3 -5]. These pressures are amplified in the context of Madagascar's growing human population and global climate change, resulting in increased contact among wildlife, humans and domesticated animals [6][7][8]. The demographic effects of these pressures have likely influenced pathogen transmission within wild lemurs and may negatively impact the health and long-term survival of these endangered species, but also alter dynamics of disease transmission between wildlife and humans.…”

“…The demographic effects of these pressures have likely influenced pathogen transmission within wild lemurs and may negatively impact the health and long-term survival of these endangered species, but also alter dynamics of disease transmission between wildlife and humans. Empirical data from Madagascar show elevated parasite densities in several lemur species and spillover of pathogenic enterobacteria and viruses from domesticated species and humans into wild lemurs [4,6,[8][9][10]. Relatively few studies, however, have focused on pathogen discovery in lemurs and none has implemented modern nextgeneration disease surveillance methods [1,11,12].…”