David T. S. Hayman

A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?

Bats are the natural reservoirs of a number of high-impact viral zoonoses. We present a quantitative analysis to address the hypothesis that bats are unique in their propensity to host zoonotic viruses based on a comparison with rodents, another important host order. We found that bats indeed host more zoonotic viruses per species than rodents, and we identified life-history and ecological factors that promote zoonotic viral richness. More zoonotic viruses are hosted by species whose distributions overlap with a greater number of other species in the same taxonomic order (sympatry). Specifically in bats, there was evidence for increased zoonotic viral richness in species with smaller litters (one young), greater longevity and more litters per year. Furthermore, our results point to a new hypothesis to explain in part why bats host more zoonotic viruses per species: the stronger effect of sympatry in bats and more viruses shared between bat species suggests that interspecific transmission is more prevalent among bats than among rodents. Although bats host more zoonotic viruses per species, the total number of zoonotic viruses identified in bats (61) was lower than in rodents (68), a result of there being approximately twice the number of rodent species as bat species. Therefore, rodents should still be a serious concern as reservoirs of emerging viruses. These findings shed light on disease emergence and perpetuation mechanisms and may help lead to a predictive framework for identifying future emerging infectious virus reservoirs.

Evidence of henipavirus infection in West African fruit bats.

Henipaviruses are emerging RNA viruses of fruit bat origin that can cause fatal encephalitis in man. Ghanaian fruit bats (megachiroptera) were tested for antibodies to henipaviruses. Using a Luminex multiplexed microsphere assay, antibodies were detected in sera of Eidolon helvum to both Nipah (39%, 95% confidence interval: 27–51%) and Hendra (22%, 95% CI: 11–33%) viruses. Virus neutralization tests further confirmed seropositivity for 30% (7/23) of Luminex positive serum samples. Our results indicate that henipavirus is present within West Africa.

Filoviruses in Bats: Current Knowledge and Future Directions

Filoviruses, including Ebolavirus and Marburgvirus, pose significant threats to public health and species conservation by causing hemorrhagic fever outbreaks with high mortality rates. Since the first outbreak in 1967, their origins, natural history, and ecology remained elusive until recent studies linked them through molecular, serological, and virological studies to bats. We review the ecology, epidemiology, and natural history of these systems, drawing on examples from other bat-borne zoonoses, and highlight key areas for future research. We compare and contrast results from ecological and virological studies of bats and filoviruses with those of other systems. We also highlight how advanced methods, such as more recent serological assays, can be interlinked with flexible statistical methods and experimental studies to inform the field studies necessary to understand filovirus persistence in wildlife populations and cross-species transmission leading to outbreaks. We highlight the need for a more unified, global surveillance strategy for filoviruses in wildlife, and advocate for more integrated, multi-disciplinary approaches to understand dynamics in bat populations to ultimately mitigate or prevent potentially devastating disease outbreaks.

A framework for the study of zoonotic disease emergence and its drivers: spillover of bat pathogens as a case study

Many serious emerging zoonotic infections have recently arisen from bats, including Ebola, Marburg, SARS-coronavirus, Hendra, Nipah, and a number of rabies and rabies-related viruses, consistent with the overall observation that wildlife are an important source of emerging zoonoses for the human population. Mechanisms underlying the recognized association between ecosystem health and human health remain poorly understood and responding appropriately to the ecological, social and economic conditions that facilitate disease emergence and transmission represents a substantial societal challenge. In the context of disease emergence from wildlife, wildlife and habitat should be conserved, which in turn will preserve vital ecosystem structure and function, which has broader implications for human wellbeing and environmental sustainability, while simultaneously minimizing the spillover of pathogens from wild animals into human beings. In this review, we propose a novel framework for the holistic and interdisciplinary investigation of zoonotic disease emergence and its drivers, using the spillover of bat pathogens as a case study. This study has been developed to gain a detailed interdisciplinary understanding, and it combines cutting-edge perspectives from both natural and social sciences, linked to policy impacts on public health, land use and conservation.

Bat flight and zoonotic viruses

High metabolism and body temperatures of flying bats might enable them to host many viruses.

Long-Term Survival of an Urban Fruit Bat Seropositive for Ebola and Lagos Bat Viruses

Ebolaviruses (EBOV) (family Filoviridae) cause viral hemorrhagic fevers in humans and non-human primates when they spill over from their wildlife reservoir hosts with case fatality rates of up to 90%. Fruit bats may act as reservoirs of the Filoviridae. The migratory fruit bat, Eidolon helvum, is common across sub-Saharan Africa and lives in large colonies, often situated in cities. We screened sera from 262 E. helvum using indirect fluorescent tests for antibodies against EBOV subtype Zaire. We detected a seropositive bat from Accra, Ghana, and confirmed this using western blot analysis. The bat was also seropositive for Lagos bat virus, a Lyssavirus, by virus neutralization test. The bat was fitted with a radio transmitter and was last detected in Accra 13 months after release post-sampling, demonstrating long-term survival. Antibodies to filoviruses have not been previously demonstrated in E. helvum. Radio-telemetry data demonstrates long-term survival of an individual bat following exposure to viruses of families that can be highly pathogenic to other mammal species. Because E. helvum typically lives in large urban colonies and is a source of bushmeat in some regions, further studies should determine if this species forms a reservoir for EBOV from which spillover infections into the human population may occur.

Bats and Lyssaviruses

Numerous bat species have been identified as important reservoirs of zoonotic viral pathogens. Rabies and rabies-related viruses constitute one of the most important viral zoonoses and pose a significant threat to public health across the globe. Whereas rabies virus (RABV) appears to be restricted to bats of the New World, related lyssavirus species have not been detected in the Americas and have only been detected in bat populations across Africa, Eurasia, and Australia. Currently, 11 distinct species of lyssavirus have been identified, 10 of which have been isolated from bat species and all of which appear to be able to cause encephalitis consistent with that seen with RABV infection of humans. In contrast, whereas lyssaviruses are apparently able to cause clinical disease in bats, it appears that these lyssaviruses may also be able to circulate within bat populations in the absence of clinical disease. This feature of these highly encephalitic viruses, alongside many other aspects of lyssavirus infection in bats, is poorly understood. Here, we review what is known of the complex relationship between bats and lyssaviruses, detailing both natural and experimental infections of these viruses in both chiropteran and nonchiropteran models. We also discuss potential mechanisms of virus excretion, transmission both to conspecifics and spill-over of virus into nonvolant species, and mechanisms of maintenance within bat populations. Importantly, we review the significance of neutralizing antibodies reported within bat populations and discuss the potential mechanisms by which highly neurovirulent viruses such as the lyssaviruses are able to infect bat species in the absence of clinical disease.

Ecology of Zoonotic Infectious Diseases in Bats: Current Knowledge and Future Directions

Bats are hosts to a range of zoonotic and potentially zoonotic pathogens. Human activities that increase exposure to bats will likely increase the opportunity for infections to spill over in the future. Ecological drivers of pathogen spillover and emergence in novel hosts, including humans, involve a complex mixture of processes, and understanding these complexities may aid in predicting spillover. In particular, only once the pathogen and host ecologies are known can the impacts of anthropogenic changes be fully appreciated. Cross‐disciplinary approaches are required to understand how host and pathogen ecology interact. Bats differ from other sylvatic disease reservoirs because of their unique and diverse lifestyles, including their ability to fly, often highly gregarious social structures, long lifespans and low fecundity rates. We highlight how these traits may affect infection dynamics and how both host and pathogen traits may interact to affect infection dynamics. We identify key questions relating to the ecology of infectious diseases in bats and propose that a combination of field and laboratory studies are needed to create data‐driven mechanistic models to elucidate those aspects of bat ecology that are most critical to the dynamics of emerging bat viruses. If commonalities can be found, then predicting the dynamics of newly emerging diseases may be possible. This modelling approach will be particularly important in scenarios when population surveillance data are unavailable and when it is unclear which aspects of host ecology are driving infection dynamics.

Ebola virus antibodies in fruit bats, Ghana, West Africa.

To the Editor: Fruit bats are the presumptive reservoir hosts of Ebola viruses (EBOVs) (genus Ebolavirus, family Filoviridae). When transmitted to humans and nonhuman primates, EBOVs can cause hemorrhagic fevers with high case-fatality rates. In 2008, we detected Zaire EBOV (ZEBOV) antibodies in a single migratory fruit bat (Eidolon helvum) from a roost in Accra, Ghana (1). This bat is common in sub-Saharan Africa and lives in large colonies, often in cities. The flight of an individual E. helvum bat during migration has been recorded as >2,500 km (2). To understand whether the single seropositive Eidolon helvum bat was evidence of EBOV circulation in the Greater Accra Region or elsewhere in sub-Saharan Africa, we tested serum of 88 nonmigratory fruit bats from the surrounding region of Ghana. Serum samples had been collected, as previously described (3,4), during May–June 2007 from fruit bats in woodland and tropical forest habitats in southern Ghana within 180 km of Accra. Initial screening for EBOV antibodies was conducted by using ELISA with a 1:1 mixture of recombinant nucleoprotein (NP) of ZEBOV and Reston EBOV (REBOV). Proteins were expressed in an Escherichia coli expression vector with a polyhistadine tag (1,5). Samples with optical density (OD) readings 3-fold above the mean OD of 2 negative control serum samples were considered EBOV-positive by ELISA. ELISA-positive samples were tested separately (at a dilution of 1:50) for reactivity against ZEBOV and REBOV NPs by using ELISA and Western blot (WB) as described (1). Each sample with positive results from both assays was retested at increasing dilutions to determine the highest dilution (endpoint titer) at which it remained positive (>3-fold above the OD for EBOV-negative sera). We detected EBOV antibodies (1:1 mixture of both NP antigens, OD>0.7) in serum samples from 32 of 88 bats (10/27 Epomops franqueti, 14/37 Epomophorus gambianus, 7/16 Hypsignathus monstrosus, 1/4 Nanonycteris veldkampii, and 0/1 Epomops buettikoferi). When tested against an individual NP, 13 of the 32 EBOV-positive serum samples were positive for EBOV (OD >0.50). Of those 13 EBOV-positive samples, 9 were ZEBOV-positive only (from 3 E. franqueti, 4 E. gambianus, and 2 H. monstrosus bats), 3 were REBOV-positive only (from 2 E. gambianus and 1 H. monstrosus bats), and 1 sample from an E. gambianus bat was positive for both ZEBOV and REBOV. Seven samples that the EBOV NP ELISA identified as positive were also positive by WB (Table). Each WB-positive serum sample was positive for the EBOV antigen that it had been most reactive against in the ELISA: 5 WB test results were positive for ZEBOV (2 of those samples also bound to REBOV), and 2 bound to REBOV only. Serum samples with positive OD values at endpoint dilutions >1:50 were definitively positive by WB; whereas those with positive OD values at and endpoint dilution of 1:50 only could be positive, negative, or equivocal by WB (Table). Table ZEBOV- and REBOV-specific results of ELISA and Western blot analysis of serum from Ebola virus–positive fruit bats, Ghana* Previous serum and viral antigen tests indicated the presence of EBOV among 2 of these bat species (E. franqueti and H. monstrosus) in Gabon, located in central Africa (6). Two others (E. gambianus and N. veldkampii) were not previously identified as potential reservoirs. Because these are nonmigratory fruit bats, our findings demonstrate that at least 1 serotype of EBOV circulates in bats in the Upper Guinean forest ecosystem in West Africa. These data might provide evidence that Tai Forest EBOV (TEBOV), formerly known as Cote d’Ivoire EBOV, circulates in this ecosystem among bats native to West Africa (7). EBOV antibody titers are highly correlated (8), but using TEBOV antigen might increase seroprevalence if TEBOV is the circulating virus. However, geographic location does not necessarily determine EBOV genetic relationships (9), and lack of cross-reactivity between serum samples positive for REBOV and ZEBOV in our study might indicate that divergent viruses circulate regionally, given phylogenetic and antigenic relationships between EBOV species (7–10). We detected a relatively high proportion of EBOV-seropositive fruit bats in a relatively small sample size of mixed species. We suggest that the prevalence of EBOV in these tested bat species is greater than that previously detected in E. helvum bats (1/262 serum samples) (1). The higher estimated prevalence in these species occurred despite the fact that E. helvum bats live in large colonies comprising several million animals, which make the species an ideal host for acute RNA virus infections. The relatively low seroprevalence of EBOV among E. helvum bats compared with that among sympatric species is contrary to our findings for a lyssavirus and an uncharacterized henipavirus (3,4). Our results, therefore, lead us to question what factors (e.g., host, ecologic) limit EBOV circulation in straw-colored fruit bats. Virus isolation is required to characterize EBOVs circulating among fruit bats in Ghana, and additional testing, including longitudinal sampling of bats, is required to further investigate the epidemiology of EBOV in West Africa. Possible public health threats should also be investigated and addressed. These initial findings, however, suggest that the risk for human infection with EBOV might be greater from bat-human contact in rural and forest settings than from urban-roosting E. helvum bats.

Behavior of bats at wind turbines

Significance Bats are dying in unprecedented numbers at wind turbines, but causes of their susceptibility are unknown. Fatalities peak during low-wind conditions in late summer and autumn and primarily involve species that evolved to roost in trees. Common behaviors of “tree bats” might put them at risk, yet the difficulty of observing high-flying nocturnal animals has limited our understanding of their behaviors around tall structures. We used thermal surveillance cameras for, to our knowledge, the first time to observe behaviors of bats at experimentally manipulated wind turbines over several months. We discovered previously undescribed patterns in the ways bats approach and interact with turbines, suggesting behaviors that evolved at tall trees might be the reason why many bats die at wind turbines. Wind turbines are causing unprecedented numbers of bat fatalities. Many fatalities involve tree-roosting bats, but reasons for this higher susceptibility remain unknown. To better understand behaviors associated with risk, we monitored bats at three experimentally manipulated wind turbines in Indiana, United States, from July 29 to October 1, 2012, using thermal cameras and other methods. We observed bats on 993 occasions and saw many behaviors, including close approaches, flight loops and dives, hovering, and chases. Most bats altered course toward turbines during observation. Based on these new observations, we tested the hypotheses that wind speed and blade rotation speed influenced the way that bats interacted with turbines. We found that bats were detected more frequently at lower wind speeds and typically approached turbines on the leeward (downwind) side. The proportion of leeward approaches increased with wind speed when blades were prevented from turning, yet decreased when blades could turn. Bats were observed more frequently at turbines on moonlit nights. Taken together, these observations suggest that bats may orient toward turbines by sensing air currents and using vision, and that air turbulence caused by fast-moving blades creates conditions that are less attractive to bats passing in close proximity. Tree bats may respond to streams of air flowing downwind from trees at night while searching for roosts, conspecifics, and nocturnal insect prey that could accumulate in such flows. Fatalities of tree bats at turbines may be the consequence of behaviors that evolved to provide selective advantages when elicited by tall trees, but are now maladaptive when elicited by wind turbines.