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The diversity and geographical distribution of fleas parasitizing small mammals have been poorly investigated on Indian Ocean islands with the exception of Madagascar where endemic plague has stimulated extensive research on these arthropod vectors. In the context of an emerging flea-borne murine typhus outbreak that occurred recently in Reunion Island, we explored fleas' diversity, distribution and host specificity on Reunion Island. Small mammal hosts belonging to five introduced species were trapped from November 2012 to November 2013 along two altitudinal transects, one on the windward eastern and one on the leeward western sides of the island. A total of 960 animals were trapped, and 286 fleas were morphologically and molecularly identified. Four species were reported: (i) two cosmopolitan Xenopsylla species which appeared by far as the prominent species, X. cheopis and X. brasiliensis; (ii) fewer fleas belonging to Echidnophaga gallinacea and Leptopsylla segnis. Rattus rattus was found to be the most abundant host species in our sample, and also the most parasitized host, predominantly by X. cheopis. A marked decrease in flea abundance was observed during the cool-dry season, which indicates seasonal fluctuation in infestation. Importantly, our data reveal that flea abundance was strongly biased on the island, with 81% of all collected fleas coming from the western dry side and no Xenopsylla flea collected on almost four hundred rodents trapped along the windward humid eastern side. The possible consequences of this sharp spatio-temporal pattern are discussed in terms of flea-borne disease risks in Reunion Island, particularly with regard to plague and the currently emerging murine typhus outbreak. Author Summary: Fleas are blood-feeding parasites involved in the transmission of several arthropod borne pathogens. Rat-fleas (Xenopsylla spp.) are known vectors of bubonic plague together with other human diseases receiving less attention such as murine typhus. This latter disease was recorded for the first time in 2011 on Reunion Island where seven human cases were further confirmed within the following year. The outbreak motivated a large survey of fleas, as these insects of major veterinary and medical importance have never been investigated on this oceanic island. We collected fleas on almost 1000 small wild mammals trapped on two altitudinal transects along the humid eastern and dry western sides of the island. Our data reveal the presence of four cosmopolitan flea species and shows an astonishing distribution pattern: 81% of all collected fleas were sampled on the western transect while not a single rat-flea was sampled on the eastern humid side of the island. Interestingly, this distribution did at least in part overlay the map of murine typhus human cases. These data stimulate the need for a diagnosis of pathogens in natural flea populations together with a comprehensive distribution map of fleas, allowing a risk assessment of flea-borne diseases in humans. [ABSTRACT FROM AUTHOR]