Illustrating the post-introduction ecology of Rift Valley fever virus in the United States of America

Abstract

Rapid urbanization, increasing international travel, and our changing climate are modifying the existing interspecies interactions at the interfaces between human, wildlife, and livestock interfaces, increasing the potential for outbreaks and transboundary disease introductions. It is more important than ever to maintain proactive research programs that integrate data across disciplines to maintain a working knowledge the potential transmission cycles of high-threat pathogens in novel environments. For vector-borne pathogens, entomological parameters, as well as interactions with the pathogen and host are highly informative, while representing avenues for control prior to an introduction. The work of this dissertation seeks to inform the potential transmission cycles of Rift Valley fever virus (RVFV) in the United States. Currently restricted to Africa and the Arabian Peninsula, RVFV infects domestic ruminants and humans with substantial degrees of morbidity and mortality. Throughout its current range, transmission involves a diversity of vectors, which are capable of transmitting the virus horizontally between vertebrates and vertically to mosquito progeny. The ecology of RVFV presents a great deal of complexity, with many unknown factors such as the roles of wildlife hosts, and relative contributions of vectors to transmission. To gain some insight into the potential ecology of RVFV in the United States, we first performed extensive sampling of mosquitoes at feedlots in northern Colorado to explore the potential for these operations to act as amplification foci after an introduction. We discovered that the most competent mosquito in Colorado that has been tested to date is highly abundant, and feeds readily on cattle, making these operations high risk for an epizootic. In this previous study we also identified blood-feeding on deer for some mosquitoes (Ae. vexans, Ae. melanimon, Ae. dorsalis) as well as domestic ruminants. We then set out to determine whether Ae. melanimon is capable of transmitting RVFV biologically, as there were no data to date for this species. We conducted infection experiments with these three Aedes species and others to determine the efficiencies with which they can transmit RVFV horizontally and vertically. We found substantial evidence for horizontal transmission and susceptibility of ovaries to infection, a prerequisite for vertical transmission, in all species but for Aedes increpitus. For these data we also developed a model to estimate the infection susceptibilities and barriers in mosquito organs in a functional manner. Finally, we sought to investigate the potential for transmission of RVFV in white-tailed deer by describing the community of mosquitoes in a riparian woodland habitat. We revealed some interesting patterns in the abundances of some mosquito species which stood in contrast to those observed at the feedlots. Several mosquito species exhibited the capacity to feed on white-tailed deer, including Ae. increpitus and Ae. vexans, both previously shown the ability to transmit RVFV by bite. By scoring the digestive stage of the blood meals in mosquitoes that were later identified to vertebrate source species, we uncovered an interesting pattern suggestive of interrupted feeding on eastern cottontail rabbits, in contrast to blood meals taken from white-tailed deer, from which mosquitoes fed to repletion. The implications of interrupted feeding for transmission by mosquitoes is unclear, but highlights the important factor of behavioral interactions between mosquito vectors and hosts which is often overlooked.