Cross-species transmission of pathogens can be facilitated by frequent contact among wildlife. Cross-species transmission is often driven by phylogenetic similarity between host species, but the role this plays when multiple host species co-roost is unknown. We developed a generalizable framework for understanding how cross-species transmission is driven by contact among co-roosting species spanning evolutionary similarities and the net impact on roost-level infection prevalence. We developed ordinary differential equation models describing population and infection dynamics between two and three co-roosting species. We derived conditions for pathogen invasion and parameterized models using co-roosting Neotropical bat systems, with interspecific transmission exponentially declining with phylogenetic distance. To assess the relative contribution of contact rates and phylogenetic similarity, we co-varied intraspecific transmission rates and phylogenetic distances while considering sensitivity to epidemiological structure and pathogen traits. For both susceptible-infected-recovered-susceptible and susceptible-infected-latent-infected models, we show that relatedness between co-roosting hosts facilitates pathogen invasion, particularly for poorly transmissible pathogens with short durations of infection and immunity or latency. These models converged on similar equilibria, and roost-level prevalence was greatest when hosts were most closely related. However, we also identified regions of parameter space where roost-level prevalence increased when hosts were distantly related. Our generalizable models are adaptable to other co-roosting systems with low-virulence pathogens that are directly transmitted and inform our understanding of pathogen spillover.
Bats display diverse foraging strategies both within and among species, and this variation can facilitate exposure to and intake of various potentially harmful contaminants (including pesticides and heavy metals) and parasites (including microparasites and macroparasites). Whereas prior work has largely focused on how dietary habits across bat species shape broad patterns of contaminant intake and, to a lesser degree, that of parasites, critical unanswered questions remain about the causal interactions between foraging, contaminants, and infection. Here, we review how bat foraging ecology shapes intake of contaminants and parasites before addressing evidence to date for their diverse impacts on bats and possible feedback loops. We outline a mechanistic framework grounded in the basic reproductive number from epidemiology for considering the health impacts of contaminants and parasites on bats and how the intake of either could influence exposure or susceptibility to the other. We also identify future research directions to better explore interrelationships among foraging, contaminants, and infection. These include but are not limited to coupling isotope, metabarcoding, and tracking techniques to assess dietary exposure; surveying emerging contaminants as well as undersampled bat species and geographies; integrating study designs such as captive experiments and mark–recapture approaches to establish causality; and expanding mathematical modeling frameworks to explore complex interactions and their validation with field data on infection. Such advances will improve our understanding of how foraging drives contaminant and infection dynamics in wild bats and their impacts on bat health, zoonotic risk, and conservation practice.
Contaminant exposure can harm wildlife. However, measuring contaminant exposure in wildlife can be challenging due to accessibility of species and/or sampling tissue matrices needed to answer research questions regarding exposure. For example, in bats and other taxa that roost, it may be best to collect pooled feces from colonies for minimal disturbance to species of conservation concern, but fecal contaminant concentrations do not provide contaminant bioaccumulation estimates. Thus, there is a need for quantifying relationships between sample matrices for measuring contaminant exposure to answer research questions pertaining to wildlife health and addressing conservation needs. Our goal was to determine relationships between fecal and fur total mercury (THg). To do so, we collected paired feces and fur from Mexican free-tailed bats (Tadarida brasiliensis) in summer 2023 in western Oklahoma at a maternity roost with no known Hg point source. We analyzed THg in each sample matrix for each individual (n = 48). We found no relationship between individual fecal and fur THg. However, when averaged, fur THg was 6.11 times greater than fecal THg. This factor can be used as a screening-level risk assessment of under-roost feces, which could then be followed by direct assessments of fur THg concentrations and health impacts. We encourage the use of this conversion factor across other insectivorous bat species and sites for estimating initial risks of contaminant exposure with minimal disturbance to species of conservation concern, when timely research for conservation actions are needed, and when a contaminant point source is not yet known.
Emerging infectious diseases threaten wildlife globally. While the effects of infectious diseases on hosts with severe infections and high mortality rates often receive considerable attention, effects on hosts that persist despite infection are less frequently studied. To understand how persisting host populations change in the face of disease, we quantified changes to the capture rates of Eptesicus fuscus (big brown bats), a persisting species susceptible to infection by the invasive fungal pathogen Pseudogymnoascus destructans (Pd; causative agent for white-nose syndrome), across the eastern US using a 30-year dataset. Capture rates of male and female E. fuscus increased from preinvasion to pathogen establishment years, with greater increases to the capture rates of females than males. Among females, capture rates of pregnant and post-lactating females increased by pathogen establishment. We outline potential mechanisms for these broad demographic changes in E. fuscus capture rates (i.e., increases to foraging from energy deficits created by Pd infection, increases to relative abundance, or changes to reproductive cycles), and suggest future research for identifying mechanisms for increasing capture rates across the eastern US. These data highlight the importance of understanding how populations of persisting host species change following pathogen invasion across a broad spatial scale. Understanding changes to population composition following pathogen invasion can identify broad ecological patterns across space and time, and open new avenues for research to identify drivers of those patterns.
Hemotropic mycoplasmas are emerging as a model system for studying bacterial pathogens in bats, but taxonomic coverage of sampled host species remains biased. We leveraged a long-term field study in Belize to uncover novel hemoplasma diversity in bats by analyzing 80 samples from 19 species, most of which are infrequently encountered. PCR targeting the partial 16S rRNA gene found 41% of bats positive for hemoplasmas. Phylogenetic analyses found two novel host shifts of hemoplasmas, four entirely new hemoplasma genotypes, and the first hemoplasma detections in four bat species. One of these novel hemoplasmas (from Neoeptesicus furinalis ) shared 97.6% identity in the partial 16S rRNA gene to a human hemoplasma ( Candidatus Mycoplasma haemohominis). Additional analysis of the partial 23S rRNA gene allowed us to also designate two novel hemoplasma species, in Myotis elegans and Phyllostomus discolor , with the proposed names Candidatus Mycoplasma haematomyotis sp. nov. and Candidatus Mycoplasma haematophyllostomi sp. nov., respectively. Our analyses show that additional hemoplasma diversity in bats can be uncovered by targeting rare or undersampled host species.
Invasive pathogens threaten wildlife health and biodiversity. Physiological responses of species highly susceptible to pathogen infections following invasion are well described. However, the responses of less susceptible species (relative to highly susceptible species) are not well known. Latitudinal gradients, which can influence body condition via Bergmann's rule and/or reflect the time it takes for an introduced pathogen to spread geographically, add an additional layer for how mammalian species respond to pathogen exposure. Our goal was to understand how hosts less susceptible to pathogen infections respond to long-term pathogen exposure across a broad latitudinal gradient. We examined changes in body mass throughout pathogen exposure time across the eastern United States (latitude ranging 30.5 degrees N-44.8 degrees N) in Eptesicus fuscus , a bat species classified as less susceptible to infection (relative to highly susceptible species) by the invasive fungal pathogen that causes white-nose syndrome, Pseudogymnoascus destructans (Pd). Using 30 years of spring through fall adult capture records, we created linear mixed-effects models for female and male bats to determine how mass or mass variation changed across the eastern United States from pre -Pd invasion years through Pd invasion (0-1 years with Pd), epidemic (2-4 years with Pd), and established years (5+ years with Pd). By Pd establishment, all female and male bats decreased body mass with increasing latitude across a spatial threshold at 39.6 degrees N. Differences in bat mass north and south of the spatial threshold progressively increased over Pd exposure time-steps such that body mass was lower in northern latitudes compared to southern latitudes by Pd establishment. Results indicated that the progressive differences in E. fuscus body mass with latitude across the eastern United States are due to long-term pathogen exposure; however, other environmental and ecological pressures may contribute to decreases in E. fuscus body mass with latitude and long-term pathogen exposure. As pathogen introductions and emerging infectious diseases become more prevalent on the landscape, it is imperative that we understand how less susceptible species directly and indirectly respond to long-term pathogen exposure in order to maintain population health in surviving species.
Emerging infectious diseases threaten wildlife populations. Without well monitored wildlife systems, it is challenging to determine accurate population and ecosystem losses following disease emergence. North American temperate bats present a unique opportunity for studying the broad impacts of wildlife disease emergence, as their federal monitoring programs were prioritized in the USA throughout the 20th century and they are currently threatened by the invasive fungal pathogen, Pseudogymnoascus destructans (Pd), which causes white-nose syndrome. Here we provide a long-term dataset for capture records of Eptesicus fuscus (big brown bat) across the eastern USA, spanning 16 years before and 14 years after Pd invasion into North America. These data represent 30,496 E. fuscus captures across 3,567 unique sites. We encourage the use of this dataset for quantifying impacts of wildlife disease and other threats to wildlife (e.g., climate change) with the incorporation of other available data. We welcome additional data contributions for E. fuscus captures across North and Central America as well as the inclusion of other variables into the dataset that contribute to the quantification of wildlife health.
Many temperate small mammals use heterothermy as a strategy to combat the energy costs of maintaining a high body temperature (Tb) during cold periods. Thus, heterothermy is a balancing act for small mammal energy conservation with the benefits of endothermy, and is variable depending on environmental factors such as ambient temperature (TA) and food availability. In temperate bat species, heterothermy is typically viewed as two distinct categories: torpid or euthermic. However, when a temperate bat undergoes acclimation to a new environment, such as captivity, it is possible for torpor and euthermia to become less distinct and instead reflect a range of Tb across TA. We hypothesized that captive big brown bats (Eptesicus fuscus) would have skin temperatures (Tskin) and metabolic rates at varying TA ranging between those of wild big brown bats in torpor and euthermia. To record captive metabolic rates by open flow respirometry, we used 11 big brown bats housed for > 6 years at Northeast Ohio Medical University (Rootstown, OH). We recorded metabolic rates at TA of 0, 5, 10, 15, 20, 25, 30, 35, and 37.5 ℃. For wild big brown bat comparisons, we extracted data for TA, Tb and metabolic rates from primary literature. We categorized wild bat Tb and metabolic rates as ‘torpid’ or ‘euthermic’ as indicated by authors within the literature. For captive bats, we labeled Tskin and metabolic rates as ‘unknown’ to eliminate our own bias on obscure values for statistical analyses. To determine differences across these categories, we created two separate linear models for 1) Tb and Tskin and 2) mass‐specific metabolic rates as functions of an interaction between TA and thermoregulatory categories. We used analysis of variance and Tukey tests to determine if this interaction explained Tb and Tskin and mass‐specific metabolic rates, and what thermoregulatory categories drove those effects, respectively. TA and thermoregulatory categories described differences between wild (‘torpid’ and ‘euthermic’) and captive (‘unknown’) big brown bats for Tb and Tskin (P < 0.0001) and mass‐specific metabolic rates (P < 0.0001). Across all TA, wild ‘euthermic’ big brown bats had greater Tb than Tskin of captive ‘unknown’ bats (P < 0.0001), and captive ‘unknown’ bats had greater Tskin than Tb of wild ‘torpid’ bats (P < 0.0001). Similarly, wild ‘euthermic’ big brown bats had greater mass‐specific metabolic rates than those of captive ‘unknown’ bats (P < 0.0001), and captive ‘unknown’ bats had greater mass‐specific metabolic rates than wild ‘torpid’ bats (P < 0.0001). This suggests captive big brown bats experienced an intermediate hypothermia and hypometabolism compared with the torpor or euthermia of wild bats. Intermediate hypothermia and hypometabolism has not yet been described in primary literature in a temperate bat species. Future research will need to tease apart differences between general effects of captivity and temperature acclimation on captive big brown bats. Our work highlights that the spectrum of heterothermy in temperate small mammals extends to big brown bats and their variability in energy conservation strategies.
Emerging pathogens can cause mass mortalities in susceptible species. High host mortality, in turn, can alter species composition, community structure and function. White-nose syndrome (WNS) is an emerging wildlife disease introduced to North America that has decimated millions of cave-dependent bats. For areas affected by WNS, there have been reports of community compositional changes, but compensatory changes to species composition following WNS has only been suggested, not reported. To determine if compensatory changes to species composition occur following WNS, we used seven years of data from statewide citizen science mobile bat acoustic routes initiated by the Ohio Division of Wildlife in 2011. We hypothesized that migratory bat abundance increased and cave-dependent bat abundance decreased following the emergence of WNS in the study period (2011–2017). Our hypothesis was based on the higher susceptibility of cave-dependent bats than migratory bats to infection and WNS mortality. We used two sets of models to identify abundance trends of each species found in Ohio and species grouped by wintering and roosting behaviors that are putatively important to changes in species composition post-WNS. Following WNS, we found a compensatory change in species in summer months from cave-dependent, cavity-roosting species (Myotis species and Eptesicus fuscus) to migratory, cavity-roosting species (Nycticeius humeralis and Lasionycteris noctivagans). However, for species that roost in foliage in the summer, we did not detect an increase in migratory species (Lasiurus borealis and Lasiurus cinereus) paired with a decrease in cave-dependent species (Perimyotis subflavus). The observed post-WNS trends in bat populations could suggest shifts in bat species composition in other areas where WNS is established.