Host and viral ecology determine bat rabies seasonality and maintenance

Abstract

Rabies is an acute viral infection that is typically fatal. Most rabies modeling has focused on disease dynamics and control within terrestrial mammals (e.g., raccoons and foxes). As such, rabies in bats has been largely neglected until recently. Because bats have been implicated as natural reservoirs for several emerging zoonotic viruses, including SARS-like corona viruses, henipaviruses, and lyssaviruses, understanding how pathogens are maintained within a population becomes vital. Unfortunately, little is known about maintenance mechanisms for any pathogen in bat populations. We present a mathematical model parameterized with unique data from an extensive study of rabies in a Colorado population of big brown bats (Eptesicus fuscus) to elucidate general maintenance mechanisms. We propose that life history patterns of many species of temperate-zone bats, coupled with sufficiently long incubation periods, allows for rabies virus maintenance. Seasonal variability in bat mortality rates, specifically low mortality during hibernation, allows long-term bat population viability. Within viable bat populations, sufficiently long incubation periods allow enough infected individuals to enter hibernation and survive until the following year, and hence avoid an epizootic fadeout of rabies virus. We hypothesize that the slowing effects of hibernation on metabolic and viral activity maintains infected individuals and their pathogens until susceptibles from the annual birth pulse become infected and continue the cycle. This research provides a context to explore similar host ecology and viral dynamics that may explain seasonal patterns and maintenance of other bat-borne diseases. chiroptera | pathogen persistence | torpor M any aspects of wildlife biology are strongly seasonal, including population dynamics of wildlife diseases (1, 2). Although mechanisms of seasonal variation of human pathogens have been well explored (3), the mechanisms for seasonality of wildlife diseases are not as well understood. Rabies virus dynamics in temperate zone bat populations exhibit a strong seasonal pattern in the number of rabies cases (Fig. 1), unlike mammalian carnivores (4). Previous analyses of bat rabies virus (BRV) using passive surveillance samples have demonstrated a higher prevalence in the spring, but especially during autumn, throughout the United States (5). However, no definitive mechanism for the seasonal pattern of rabies in bats has been described. In addition, how rabies virus is maintained within bat populations remains unclear. Here, we explore factors that drive pathogen maintenance and simultaneously explain the unique seasonal patterns of rabies in bats.Each year, rabies virus infection causes in excess of 55,000 human deaths globally, mostly from dog bites in developing countries (6). Successful vaccination programs of domesticated animals have virtually eliminated dog rabies in North America over the past 50 y, and more recent vaccination strategies for wildlife populations have controlled rabies virus in other carniv...

Biannual birth pulses allow filoviruses to persist in bat populations

“…Infection prevalence of other viruses, including coronaviruses and rabies, shows seasonal dynamics in bats [25][26][27]. The increase in susceptible hosts and contact rates during and following the birthing period may drive infection dynamics [28], though overwinter hibernation has also been shown to be important in temperate bat systems for rabies [29]. Amman et al [24] identified MARV in Rousettus aegyptiacus bats in a cave in Uganda by using polymerase chain reaction (PCR) and viral isolation, and discovered that the disease occurred in pulses in older juvenile bats (approx.…”

Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats

“…Understanding viral persistence in bat populations is challenging because seemingly ideal ecological traits for explosive pathogen transmission such as high mobility and colonial aggregation contrast with the limited supply of new susceptible individuals generated by characteristically long-lived and slow-reproducing host species. Consequently, epizootiological models of bat viruses have required complex immunological or behavioral mechanisms to achieve long-term persistence, such as waning maternal immunity or an extended incubation period through hibernation (4)(5)(6). These studies also demonstrated the power of a combined field, experimental, and modeling approach for identifying persistence mechanisms in bats, but such holistic investigations are still absent for most systems (3).…”

Geographic distribution of <em>Desmodus rotundus</em> in Mexico under current and future climate change scenarios: Implications for bovine paralytic rabies infection

“…14,16 Some studies suggest that if climatic conditions change, individuals are likely to relocate to new areas and roosts. 18,19 Due to its ecological plasticity, the vampire bat can easily adapt to new landscapes modified by humans where loss of native plant cover, increased forage and greater abundance of domestic livestock have created suitable conditions for their breeding and feeding. 4,8 In Mexico, it is expected that the combination of changes in land use and changes in global and regional climates will produce species distributional shifts, including reservoirs and vectors for infectious diseases, modifying the patterns of infectious Climate change on bovine paralytic rabies in Mexico DOI: http://dx.doi.org/10.21753/vmoa.…”