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1.  Susceptibility and Pathogenesis of Little Brown Bats (Myotis lucifugus) to Heterologous and Homologous Rabies Viruses 
Journal of Virology  2013;87(16):9008-9015.
Rabies virus (RABV) maintenance in bats is not well understood. Big brown bats (Eptesicus fuscus), little brown bats (Myotis lucifugus), and Mexican free-tailed bats (Tadarida brasiliensis) are the most common bats species in the United States. These colonial bat species also have the most frequent contact with humans and domestic animals. However, the silver-haired bat (Lasionycteris noctivagans) RABV is associated with the majority of human rabies virus infections in the United States and Canada. This is of interest because silver-haired bats are more solitary bats with infrequent human interaction. Our goal was to determine the likelihood of a colonial bat species becoming infected with and transmitting a heterologous RABV. To ascertain the potential of heterologous RABV infection in colonial bat species, little brown bats were inoculated with a homologous RABV or one of two heterologous RABVs. Additionally, to determine if the route of exposure influenced the disease process, bats were inoculated either intramuscularly (i.m.) or subcutaneously (s.c.) with a homologous or heterologous RABV. Our results demonstrate that intramuscular inoculation results in a more rapid progression of disease onset, whereas the incubation time in bats inoculated s.c. is significantly longer. Additionally, cross protection was not consistently achieved in bats previously inoculated with a heterologous RABV following a challenge with a homologous RABV 6 months later. Finally, bats that developed rabies following s.c. inoculation were significantly more likely to shed virus in their saliva and demonstrated increased viral dissemination. In summary, bats inoculated via the s.c. route are more likely to shed virus, thus increasing the likelihood of transmission.
PMCID: PMC3754046  PMID: 23741002
2.  Climate and Weather Impact Timing of Emergence of Bats 
PLoS ONE  2012;7(8):e42737.
Interest in forecasting impacts of climate change have heightened attention in recent decades to how animals respond to variation in climate and weather patterns. One difficulty in determining animal response to climate variation is lack of long-term datasets that record animal behaviors over decadal scales. We used radar observations from the national NEXRAD network of Doppler weather radars to measure how group behavior in a colonially-roosting bat species responded to annual variation in climate and daily variation in weather over the past 11 years. Brazilian free-tailed bats (Tadarida brasiliensis) form dense aggregations in cave roosts in Texas. These bats emerge from caves daily to forage at high altitudes, which makes them detectable with Doppler weather radars. Timing of emergence in bats is often viewed as an adaptive trade-off between emerging early and risking predation or increased competition and emerging late which restricts foraging opportunities. We used timing of emergence from five maternity colonies of Brazilian free-tailed bats in south-central Texas during the peak lactation period (15 June–15 July) to determine whether emergence behavior was associated with summer drought conditions and daily temperatures. Bats emerged significantly earlier during years with extreme drought conditions than during moist years. Bats emerged later on days with high surface temperatures in both dry and moist years, but there was no relationship between surface temperatures and timing of emergence in summers with normal moisture levels. We conclude that emergence behavior is a flexible animal response to climate and weather conditions and may be a useful indicator for monitoring animal response to long-term shifts in climate.
PMCID: PMC3411708  PMID: 22876331
3.  High Diversity of Rabies Viruses Associated with Insectivorous Bats in Argentina: Presence of Several Independent Enzootics 
Rabies is a fatal infection of the central nervous system primarily transmitted by rabid animal bites. Rabies virus (RABV) circulates through two different epidemiological cycles: terrestrial and aerial, where dogs, foxes or skunks and bats, respectively, act as the most relevant reservoirs and/or vectors. It is widely accepted that insectivorous bats are not important vectors of RABV in Argentina despite the great diversity of bat species and the extensive Argentinean territory.
We studied the positivity rate of RABV detection in different areas of the country, and the antigenic and genetic diversity of 99 rabies virus (RABV) strains obtained from 14 species of insectivorous bats collected in Argentina between 1991 and 2008.
Based on the analysis of bats received for RABV analysis by the National Rabies system of surveillance, the positivity rate of RABV in insectivorous bats ranged from 3.1 to 5.4%, depending on the geographic location. The findings were distributed among an extensive area of the Argentinean territory. The 99 strains of insectivorous bat-related sequences were divided into six distinct lineages associated with Tadarida brasiliensis, Myotis spp, Eptesicus spp, Histiotus montanus, Lasiurus blosseviilli and Lasiurus cinereus. Comparison with RABV sequences obtained from insectivorous bats of the Americas revealed co-circulation of similar genetic variants in several countries. Finally, inter-species transmission, mostly related with Lasiurus species, was demonstrated in 11.8% of the samples.
This study demonstrates the presence of several independent enzootics of rabies in insectivorous bats of Argentina. This information is relevant to identify potential areas at risk for human and animal infection.
Author Summary
In Argentina, successful vaccination and control of terrestrial rabies in the 1980s revealed the importance of the aerial route in RABV transmission. Current distribution of cases shows a predominance of rabies by hematophagous bats in the Northern regions where rabies is a major public health concern; in contrast, in Central and Southern regions where rabies is not a major public health concern, little surveillance is performed. Based on the analysis of insectivorous bats received for RABV analysis by the National Rabies system of surveillance, the positivity rate of RABV in insectivorous bats in these regions ranged from 3.1 to 5.4%. This rate is comparable to other nations such as the United States (9–10%) where insectivorous bats are an important cause of concern for RABV surveillance systems. Antigenic and genetic analysis of a wide collection of rabies strains shows the presence of multiple endemic cycles associated with six bat insectivorous species distributed among an extensive area of the Argentinean territory and several countries of the Americas. Finally, inter-species transmission, mostly related with Lasiurus species, was demonstrated in 11.8% of the samples. Increased public education about the relationship between insectivorous bats and rabies are essential to avoid human cases and potential spread to terrestrial mammals.
PMCID: PMC3348165  PMID: 22590657
4.  Evolutionary History and Phylogeography of Rabies Viruses Associated with Outbreaks in Trinidad 
Bat rabies is an emerging disease of public health significance in the Americas. The Caribbean island of Trinidad experiences periodic outbreaks within the livestock population. We performed molecular characterisation of Trinidad rabies virus (RABV) and used a Bayesian phylogeographic approach to investigate the extent to which outbreaks are a result of in situ evolution versus importation of virus from the nearby South American mainland. Trinidadian RABV sequences were confirmed as bat variant and clustered with Desmodus rotundus (vampire bat) related sequences. They fell into two largely temporally defined lineages designated Trinidad I and II. The Trinidad I lineage which included sequences from 1997–2000 (all but two of which were from the northeast of the island) was most closely related to RABV from Ecuador (2005, 2007), French Guiana (1990) and Venezuela (1993, 1994). Trinidad II comprised sequences from the southwest of the island, which clustered into two groups: Trinidad IIa, which included one sequence each from 2000 and 2007, and Trinidad IIb including all 2010 sequences. The Trinidad II sequences were most closely related to sequences from Brazil (1999, 2004) and Uruguay (2007, 2008). Phylogeographic analyses support three separate RABV introductions from the mainland from which each of the three Trinidadian lineages arose. The estimated dates for the introductions and subsequent lineage expansions suggest periods of in situ evolution within Trinidad following each introduction. These data also indicate co-circulation of Trinidad lineage I and IIa during 2000. In light of these findings and the likely vampire bat origin of Trinidadian RABV, further studies should be conducted to investigate the relationship between RABV spatiotemporal dynamics and vampire bat population ecology, in particular any movement between the mainland and Trinidad.
Author Summary
The Caribbean island of Trinidad experiences periodic rabies virus (RABV) outbreaks within the livestock population. In this study, we inferred the evolutionary history of RABV in the Americas and reconstructed past patterns of RABV geographic spread in order to address the question of whether Trinidadian outbreaks arise from locally maintained RABV or are the result of virus importation from the mainland (presumably via infected bats). Our results provide statistical support for three importation events that gave rise to each of three Trinidadian vampire bat-associated lineages identified in the study. They also indicate limited periods of in situ evolution within Trinidad following each of these introductions. The results also support Mexico and Brazil as major epicenters for the expansion of RABV associated with vampire bats throughout the Americas and consequently to Trinidad. The findings of our study are particularly relevant to local RABV monitoring and control. In addition to justifying vampire bats as the main target for active rabies surveillance and control activities in Trinidad, they suggest that more intense surveillance of regions that lie close to the mainland may be warranted. Finally, in light of these findings, further studies should be conducted to investigate the relationship between RABV spatiotemporal dynamics and vampire bat population ecology.
PMCID: PMC3749974  PMID: 23991230
5.  Effects of Hierarchical Roost Removal on Northern Long-Eared Bat (Myotis septentrionalis) Maternity Colonies 
PLoS ONE  2015;10(1):e0116356.
Forest roosting bats use a variety of ephemeral roosts such as snags and declining live trees. Although conservation of summer maternity habitat is considered critical for forest-roosting bats, bat response to roost loss still is poorly understood. To address this, we monitored 3 northern long-eared bat (Myotis septentrionalis) maternity colonies on Fort Knox Military Reservation, Kentucky, USA, before and after targeted roost removal during the dormant season when bats were hibernating in caves. We used 2 treatments: removal of a single highly used (primary) roost and removal of 24% of less used (secondary) roosts, and an un-manipulated control. Neither treatment altered the number of roosts used by individual bats, but secondary roost removal doubled the distances moved between sequentially used roosts. However, overall space use by and location of colonies was similar pre- and post-treatment. Patterns of roost use before and after removal treatments also were similar but bats maintained closer social connections after our treatments. Roost height, diameter at breast height, percent canopy openness, and roost species composition were similar pre- and post-treatment. We detected differences in the distribution of roosts among decay stages and crown classes pre- and post-roost removal, but this may have been a result of temperature differences between treatment years. Our results suggest that loss of a primary roost or ≤ 20% of secondary roosts in the dormant season may not cause northern long-eared bats to abandon roosting areas or substantially alter some roosting behaviors in the following active season when tree-roosts are used. Critically, tolerance limits to roost loss may be dependent upon local forest conditions, and continued research on this topic will be necessary for conservation of the northern long-eared bat across its range.
PMCID: PMC4303276  PMID: 25611060
6.  Ecological Factors Associated with European Bat Lyssavirus Seroprevalence in Spanish Bats 
PLoS ONE  2013;8(5):e64467.
Bats have been proposed as major reservoirs for diverse emerging infectious viral diseases, with rabies being the best known in Europe. However, studies exploring the ecological interaction between lyssaviruses and their natural hosts are scarce. This study completes our active surveillance work on Spanish bat colonies that began in 1992. Herein, we analyzed ecological factors that might affect the infection dynamics observed in those colonies. Between 2001 and 2011, we collected and tested 2,393 blood samples and 45 dead bats from 25 localities and 20 bat species. The results for dead confirmed the presence of EBLV-1 RNA in six species analyzed (for the first time in Myotis capaccinii). Samples positive for European bat lyssavirus-1 (EBLV-1)–neutralizing antibodies were detected in 68% of the localities sampled and in 13 bat species, seven of which were found for the first time (even in Myotis daubentonii, a species to date always linked to EBLV-2). EBLV-1 seroprevalence (20.7%) ranged between 11.1 and 40.2% among bat species and seasonal variation was observed, with significantly higher antibody prevalence in summer (July). EBLV-1 seroprevalence was significantly associated with colony size and species richness. Higher seroprevalence percentages were found in large multispecific colonies, suggesting that intra- and interspecific contacts are major risk factors for EBLV-1 transmission in bat colonies. Although bat-roosting behavior strongly determines EBLV-1 variability, we also found some evidence that bat phylogeny might be involved in bat-species seroprevalence. The results of this study highlight the importance of life history and roost ecology in understanding EBLV-1–prevalence patterns in bat colonies and also provide useful information for public health officials.
PMCID: PMC3659107  PMID: 23700480
7.  Bat Rabies in Guatemala 
Rabies in bats is considered enzootic throughout the New World, but few comparative data are available for most countries in the region. As part of a larger pathogen detection program, enhanced bat rabies surveillance was conducted in Guatemala, between 2009 and 2011. A total of 672 bats of 31 species were sampled and tested for rabies. The prevalence of rabies virus (RABV) detection among all collected bats was low (0.3%). Viral antigens were detected and infectious virus was isolated from the brains of two common vampire bats (Desmodus rotundus). RABV was also isolated from oral swabs, lungs and kidneys of both bats, whereas viral RNA was detected in all of the tissues examined by hemi-nested RT-PCR except for the liver of one bat. Sequencing of the nucleoprotein gene showed that both viruses were 100% identical, whereas sequencing of the glycoprotein gene revealed one non-synonymous substitution (302T,S). The two vampire bat RABV isolates in this study were phylogenetically related to viruses associated with vampire bats in the eastern states of Mexico and El Salvador. Additionally, 7% of sera collected from 398 bats demonstrated RABV neutralizing antibody. The proportion of seropositive bats varied significantly across trophic guilds, suggestive of complex intraspecific compartmentalization of RABV perpetuation.
Author Summary
In this study we provide results of the first active and extensive surveillance effort for rabies virus (RABV) circulation among bats in Guatemala. The survey included multiple geographic areas and multiple species of bats, to assess the broader public and veterinary health risks associated with rabies in bats in Guatemala. RABV was isolated from vampire bats (Desmodus rotundus) collected in two different locations in Guatemala. Sequencing of the isolates revealed a closer relationship to Mexican and Central American vampire bat isolates than to South American isolates. The detection of RABV neutralizing antibodies in 11 species, including insectivorous, frugivorous, and sanguivorous bats, demonstrates viral circulation in both hematophagous and non-hematophagous bat species in Guatemala. The presence of bat RABV in rural communities requires new strategies for public health education regarding contact with bats, improved laboratory-based surveillance of animals associated with human exposures, and novel techniques for modern rabies prevention and control. Additionally, healthcare practitioners should emphasize the collection of a detailed medical history, including questions regarding bat exposure, for patients presenting with clinical syndromes compatible with rabies or any clinically diagnosed progressive encephalitis.
PMCID: PMC4117473  PMID: 25080103
8.  Chemically-Mediated Roostmate Recognition and Roost Selection by Brazilian Free-Tailed Bats (Tadarida brasiliensis) 
PLoS ONE  2009;4(11):e7781.
The Brazilian free-tailed bat (Tadarida brasiliensis) is an exceptionally social and gregarious species of chiropteran known to roost in assemblages that can number in the millions. Chemical recognition of roostmates within these assemblages has not been extensively studied despite the fact that an ability to chemically recognize individuals could play an important role in forming and stabilizing complex suites of social interactions.
Methodology/Principal Findings
Individual bats were given a choice between three roosting pouches: one permeated with the scent of a group of roostmates, one permeated with the scent of non-roostmates, and a clean control. Subjects rejected non-roostmate pouches with greater frequency than roostmate pouches or blank control pouches. Also, bats chose to roost in the roostmate scented pouches more often than the non-roostmate or control pouches.
We demonstrated that T. brasiliensis has the ability to chemically recognize roostmates from non-roostmates and a preference for roosting in areas occupied by roostmates. It is important to investigate these behaviors because of their potential importance in colony dynamics and roost choice.
PMCID: PMC2770117  PMID: 19901986
9.  Thermal Windows on Brazilian Free-tailed Bats Facilitate Thermoregulation during Prolonged Flight 
The Brazilian free-tailed bat (Tadarida brasiliensis) experiences challenging thermal conditions while roosting in hot caves, flying during warm daylight conditions, and foraging at cool high altitudes. Using thermal infrared cameras, we identified hot spots along the flanks of free-ranging Brazilian free-tailed bats, ventral to the extended wings. These hot spots are absent in syntopic cave myotis (Myotis velifer), a species that forages over relatively short distances, and does not engage in long-distance migration. We hypothesized that the hot spots, or “radiators,” on Brazilian free-tailed bats may be adaptations for migration, particularly in this long-distance, high-flying species. We examined the vasculature of radiators on Brazilian free-tailed bats with transillumination to characterize the unique arrangements of arteries and veins that are positioned perpendicular to the body in the proximal region of the wing. We hypothesized that these radiators aid in maintaining heat balance by flushing the uninsulated thermal window with warm blood, thereby dissipating heat while bats are flying under warm conditions, but shunting blood away and conserving heat when they are flying in cooler air at high altitudes. We also examined fluid-preserved specimens representing 122 species from 15 of 18 chiropteran families and radiators appeared present only in species in the family Molossidae, including both sedentary and migratory species and subspecies. Thus, the radiator appears to be a unique trait that may facilitate energy balance and water balance during sustained dispersal, foraging, and long-distance migration.
PMCID: PMC2931312  PMID: 20811514
10.  Molecular epidemiology of livestock rabies viruses isolated in the northeastern Brazilian states of Paraíba and Pernambuco from 2003 - 2009 
BMC Research Notes  2012;5:32.
Limited or no epidemiological information has been reported for rabies viruses (RABVs) isolated from livestock in the northeastern Brazilian states of Paraíba (PB) and Pernambuco (PE). The aim of this study was to clarify the molecular epidemiology of RABVs circulating in livestock, especially cattle, in these areas between 2003 and 2009.
Phylogenetic analysis based on 890 nt of the nucleoprotein (N) gene revealed that the 52 livestock-derived RABV isolates characterized here belonged to a single lineage. These isolates clustered with a vampire bat-related RABV lineage previously identified in other states in Brazil; within PB and PE, this lineage was divided between the previously characterized main lineage and a novel sub-lineage.
The occurrences of livestock rabies in PB and PE originated from vampire bat RABVs, and the causative RABV lineage has been circulating in this area of northeastern Brazil for at least 7 years. This distribution pattern may correlate to that of a vampire bat population isolated by geographic barriers.
PMCID: PMC3285087  PMID: 22243739
11.  Rabies-Related Knowledge and Practices Among Persons At Risk of Bat Exposures in Thailand 
Rabies is a fatal encephalitis caused by lyssaviruses. Evidence of lyssavirus circulation has recently emerged in Southeast Asian bats. A cross-sectional study was conducted in Thailand to assess rabies-related knowledge and practices among persons regularly exposed to bats and bat habitats. The objectives were to identify deficiencies in rabies awareness, describe the occurrence of bat exposures, and explore factors associated with transdermal bat exposures.
A survey was administered to a convenience sample of adult guano miners, bat hunters, game wardens, and residents/personnel at Buddhist temples where mass bat roosting occurs. The questionnaire elicited information on demographics, experience with bat exposures, and rabies knowledge. Participants were also asked to describe actions they would take in response to a bat bite as well as actions for a bite from a potentially rabid animal. Bivariate analysis was used to compare responses between groups and multivariable logistic regression was used to explore factors independently associated with being bitten or scratched by a bat.
Of 106 people interviewed, 11 (10%) identified bats as a potential source of rabies. A history of a bat bite or scratch was reported by 29 (27%), and 38 (36%) stated either that they would do nothing or that they did not know what they would do in response to a bat bite. Guano miners were less likely than other groups to indicate animal bites as a mechanism of rabies transmission (68% vs. 90%, p = 0.03) and were less likely to say they would respond appropriately to a bat bite or scratch (61% vs. 27%, p = 0.003). Guano mining, bat hunting, and being in a bat cave or roost area more than 5 times a year were associated with history of a bat bite or scratch.
These findings indicate the need for educational outreach to raise awareness of bat rabies, promote exposure prevention, and ensure appropriate health-seeking behaviors for bat-inflicted wounds, particularly among at-risk groups in Thailand.
Author Summary
Rabies is a fatal encephalitis caused by lyssaviruses. Evidence of lyssavirus circulation has recently emerged in Southeast Asian bats. We surveyed persons regularly exposed to bats and bat habitats in Thailand to assess rabies‐related knowledge and practices. Targeted groups included guano miners, bat hunters, game wardens, and residents/personnel at Buddhist temples where mass bat roosting occurs. Of the 106 people interviewed, 11 (10%) identified bats as a source of rabies. History of a bat bite/scratch was reported by 29 (27%), and 38 (36%) expressed either that they would do nothing or that they did not know what they would do in response to a bat bite. Guano miners were less likely than other groups to indicate animal bites as a mechanism of transmission (68% vs. 90%, p=0.03) and were less likely to say they would respond appropriately to a bat bite or scratch (61% vs. 27%, p=0.003). These findings indicate a need for educational outreach in Thailand to raise awareness of bat rabies, promote exposure prevention, and ensure health‐seeking behaviors for bat‐inflicted wounds, particularly among at‐risk groups.
PMCID: PMC3125144  PMID: 21738801
12.  Variability in Seroprevalence of Rabies Virus Neutralizing Antibodies and Associated Factors in a Colorado Population of Big Brown Bats (Eptesicus fuscus) 
PLoS ONE  2014;9(1):e86261.
In 2001–2005 we sampled permanently marked big brown bats (Eptesicus fuscus) at summer roosts in buildings at Fort Collins, Colorado, for rabies virus neutralizing antibodies (RVNA). Seroprevalence was higher in adult females (17.9%, n = 2,332) than males (9.4%, n = 128; P = 0.007) or volant juveniles (10.2%, n = 738; P<0.0001). Seroprevalence was lowest in a drought year with local insecticide use and highest in the year with normal conditions, suggesting that environmental stress may suppress RVNA production in big brown bats. Seroprevalence also increased with age of bat, and varied from 6.2 to 26.7% among adult females at five roosts sampled each year for five years. Seroprevalence of adult females at 17 other roosts sampled for 1 to 4 years ranged from 0.0 to 47.1%. Using logistic regression, the only ranking model in our candidate set of explanatory variables for serological status at first sampling included year, day of season, and a year by day of season interaction that varied with relative drought conditions. The presence or absence of antibodies in individual bats showed temporal variability. Year alone provided the best model to explain the likelihood of adult female bats showing a transition to seronegative from a previously seropositive state. Day of the season was the only competitive model to explain the likelihood of a transition from seronegative to seropositive, which increased as the season progressed. We found no rabies viral RNA in oropharyngeal secretions of 261 seropositive bats or in organs of 13 euthanized seropositive bats. Survival of seropositive and seronegative bats did not differ. The presence of RVNA in serum of bats should not be interpreted as evidence for ongoing rabies infection.
PMCID: PMC3899234  PMID: 24465996
13.  Roosting and Foraging Social Structure of the Endangered Indiana Bat (Myotis sodalis) 
PLoS ONE  2014;9(5):e96937.
Social dynamics are an important but poorly understood aspect of bat ecology. Herein we use a combination of graph theoretic and spatial approaches to describe the roost and social network characteristics and foraging associations of an Indiana bat (Myotis sodalis) maternity colony in an agricultural landscape in Ohio, USA. We tracked 46 bats to 50 roosts (423 total relocations) and collected 2,306 foraging locations for 40 bats during the summers of 2009 and 2010. We found the colony roosting network was highly centralized in both years and that roost and social networks differed significantly from random networks. Roost and social network structure also differed substantially between years. Social network structure appeared to be unrelated to segregation of roosts between age classes. For bats whose individual foraging ranges were calculated, many shared foraging space with at least one other bat. Compared across all possible bat dyads, 47% and 43% of the dyads showed more than expected overlap of foraging areas in 2009 and 2010 respectively. Colony roosting area differed between years, but the roosting area centroid shifted only 332 m. In contrast, whole colony foraging area use was similar between years. Random roost removal simulations suggest that Indiana bat colonies may be robust to loss of a limited number of roosts but may respond differently from year to year. Our study emphasizes the utility of graphic theoretic and spatial approaches for examining the sociality and roosting behavior of bats. Detailed knowledge of the relationships between social and spatial aspects of bat ecology could greatly increase conservation effectiveness by allowing more structured approaches to roost and habitat retention for tree-roosting, socially-aggregating bat species.
PMCID: PMC4016147  PMID: 24816811
14.  Ecology and Geography of Transmission of Two Bat-Borne Rabies Lineages in Chile 
Rabies was known to humans as a disease thousands of years ago. In America, insectivorous bats are natural reservoirs of rabies virus. The bat species Tadarida brasiliensis and Lasiurus cinereus, with their respective, host-specific rabies virus variants AgV4 and AgV6, are the principal rabies reservoirs in Chile. However, little is known about the roles of bat species in the ecology and geographic distribution of the virus. This contribution aims to address a series of questions regarding the ecology of rabies transmission in Chile. Analyzing records from 1985–2011 at the Instituto de Salud Pública de Chile (ISP) and using ecological niche modeling, we address these questions to help in understanding rabies-bat ecological dynamics in South America. We found ecological niche identity between both hosts and both viral variants, indicating that niches of all actors in the system are undifferentiated, although the viruses do not necessarily occupy the full geographic distributions of their hosts. Bat species and rabies viruses share similar niches, and our models had significant predictive power even across unsampled regions; results thus suggest that outbreaks may occur under consistent, stable, and predictable circumstances.
Author Summary
The situation of rabies in America has been changing: rabies in dogs has decreased considerably, but bats are increasingly documented as natural reservoirs of other rabies variants. A significant gap exists in understanding of bat-borne rabies in Latin America. We identified bat species known to be connected with enzootic rabies with different antigenic variants in Chile, and compiled large-scale data sets by which to test for ecological niche differences among virus lineages and bat hosts. Our results begin to characterize important ecological factors affecting rabies distribution; modeling rabies in Chile allows comparisons across different latitudes and diverse landscapes. We found that rabies virus strains are found in similar environments, regardless of the bat host involved. This research improves understanding of bat-borne rabies dynamics, and important step towards preventing and controlling this and other emergent diseases linked to bats.
PMCID: PMC3861194  PMID: 24349592
15.  Enzootic and Epizootic Rabies Associated with Vampire Bats, Peru 
Emerging Infectious Diseases  2013;19(9):1463-1469.
During the past decade, incidence of human infection with rabies virus (RABV) spread by the common vampire bat (Desmodus rotundus) increased considerably in South America, especially in remote areas of the Amazon rainforest, where these bats commonly feed on humans. To better understand the epizootiology of rabies associated with vampire bats, we used complete sequences of the nucleoprotein gene to infer phylogenetic relationships among 157 RABV isolates collected from humans, domestic animals, and wildlife, including bats, in Peru during 2002–2007. This analysis revealed distinct geographic structuring that indicates that RABVs spread gradually and involve different vampire bat subpopulations with different transmission cycles. Three putative new RABV lineages were found in 3 non–vampire bat species that may represent new virus reservoirs. Detection of novel RABV variants and accurate identification of reservoir hosts are critically important for the prevention and control of potential virus transmission, especially to humans.
PMCID: PMC3810916
rabies; molecular epidemiology; bats; Peru; viruses; zoonoses; vampire bats
16.  Molecular Inferences Suggest Multiple Host Shifts of Rabies Viruses from Bats to Mesocarnivores in Arizona during 2001–2009 
PLoS Pathogens  2012;8(6):e1002786.
In nature, rabies virus (RABV; genus Lyssavirus, family Rhabdoviridae) represents an assemblage of phylogenetic lineages, associated with specific mammalian host species. Although it is generally accepted that RABV evolved originally in bats and further shifted to carnivores, mechanisms of such host shifts are poorly understood, and examples are rarely present in surveillance data. Outbreaks in carnivores caused by a RABV variant, associated with big brown bats, occurred repeatedly during 2001–2009 in the Flagstaff area of Arizona. After each outbreak, extensive control campaigns were undertaken, with no reports of further rabies cases in carnivores for the next several years. However, questions remained whether all outbreaks were caused by a single introduction and further perpetuation of bat RABV in carnivore populations, or each outbreak was caused by an independent introduction of a bat virus. Another question of concern was related to adaptive changes in the RABV genome associated with host shifts. To address these questions, we sequenced and analyzed 66 complete and 20 nearly complete RABV genomes, including those from the Flagstaff area and other similar outbreaks in carnivores, caused by bat RABVs, and representatives of the major RABV lineages circulating in North America and worldwide. Phylogenetic analysis demonstrated that each Flagstaff outbreak was caused by an independent introduction of bat RABV into populations of carnivores. Positive selection analysis confirmed the absence of post-shift changes in RABV genes. In contrast, convergent evolution analysis demonstrated several amino acids in the N, P, G and L proteins, which might be significant for pre-adaptation of bat viruses to cause effective infection in carnivores. The substitution S/T242 in the viral glycoprotein is of particular merit, as a similar substitution was suggested for pathogenicity of Nishigahara RABV strain. Roles of the amino acid changes, detected in our study, require additional investigations, using reverse genetics and other approaches.
Author Summary
Host shifts of the rabies virus (RABV) from bats to carnivores are important for our understanding of viral evolution and emergence, and have significant public health implications, particularly for the areas where “terrestrial” rabies has been eliminated. In this study we addressed several rabies outbreaks in carnivores that occurred in the Flagstaff area of Arizona during 2001–2009, and caused by the RABV variant associated with big brown bats (Eptesicus fuscus). Based on phylogenetic analysis we demonstrated that each outbreak resulted from a separate introduction of bat RABV into populations of carnivores. No post-shift changes in viral genomes were detected under the positive selection analysis. Trying to answer the question why certain bat RABV variants are capable for host shifts to carnivores and other variants are not, we developed a convergent evolution analysis, and implemented it for multiple RABV lineages circulating worldwide. This analysis identified several amino acids in RABV proteins which may facilitate host shifts from bats to carnivores. Precise roles of these amino acids require additional investigations, using reverse genetics and animal experimentation. In general, our approach and the results obtained can be used for prediction of host shifts and emergence of other zoonotic pathogens.
PMCID: PMC3380930  PMID: 22737076
17.  Host immunity to repeated rabies virus infection in big brown bats 
The Journal of General Virology  2010;91(Pt 9):2360-2366.
Bats are natural reservoirs for the majority of lyssaviruses globally, and are unique among mammals in having exceptional sociality and longevity. Given these facets, and the recognized status of bats as reservoirs for rabies viruses (RABVs) in the Americas, individual bats may experience repeated exposure to RABV during their lifetime. Nevertheless, little information exists with regard to within-host infection dynamics and the role of immunological memory that may result from abortive RABV infection in bats. In this study, a cohort of big brown bats (Eptesicus fuscus) was infected intramuscularly in the left and right masseter muscles with varying doses [10−0.1–104.9 median mouse intracerebral lethal doses (MICLD50)] of an E. fuscus RABV variant isolated from a naturally infected big brown bat. Surviving bats were infected a second time at 175 days post-(primary) infection with a dose (103.9–104.9 MICLD50) of the same RABV variant. Surviving bats were infected a third time at either 175 or 305 days post-(secondary) infection with a dose (104.9 MICLD50) of the same RABV variant. When correcting for dose, similar mortality was observed following primary and secondary infection, but reduced mortality was observed following the third and last RABV challenge, despite infection with a high viral dose. Inducible RABV-neutralizing antibody titres post-infection were ephemeral among infected individuals, and dropped below levels of detection in several bats between subsequent infections. These results suggest that long-term repeated infection of bats may confer significant immunological memory and reduced susceptibility to RABV infection.
PMCID: PMC3052523  PMID: 20519458
18.  A universal real-time assay for the detection of Lyssaviruses 
Journal of Virological Methods  2011;177(1-24):87-93.
► Universal real-time PCR primer pair demonstrated to hybridize to and detect each of the known Lyssaviruses (including Rabies virus) with greater sensitivity than a standard pan-Lyssavirus hemi-nested RT-PCR typically used. ► Target sequences of bat derived virus species unavailable for analysis (Aravan-, Khujand-, Irkut-, West Caucasian bat- and Shimoni bat virus) were synthesized to produce oligonucleotides and the synthetic DNA was used as a target for primer hybridization.
Rabies virus (RABV) is enzootic throughout most of the world. It is now widely accepted that RABV had its origins in bats. Ten of the 11 Lyssavirus species recognised, including RABV, have been isolated from bats. There is, however, a lack of understanding regarding both the ecology and host reservoirs of Lyssaviruses. A real-time PCR assay for the detection of all Lyssaviruses using universal primers would be beneficial for Lyssavirus surveillance. It was shown that using SYBR® Green, a universal real-time PCR primer pair previously demonstrated to detect European bat Lyssaviruses 1 and 2, and RABV, was able to detect reverse transcribed RNA for each of the seven virus species available to us. Target sequences of bat derived virus species unavailable for analysis were synthesized to produce oligonucleotides. Lagos Bat-, Duvenhage- and Mokola virus full nucleoprotein gene clones enabled a limit of 5–50 plasmid copies to be detected. Five copies of each of the synthetic DNA oligonucleotides of Aravan-, Khujand-, Irkut-, West Caucasian bat- and Shimoni bat virus were detected. The single universal primer pair was therefore able to detect each of the most divergent known Lyssaviruses with great sensitivity.
PMCID: PMC3191275  PMID: 21777619
Lyssavirus; Rabies; Bat; SYBR Green; Real-time PCR; Synthetic DNA
19.  Rabies Virus Infection in Eptesicus fuscus Bats Born in Captivity (Naïve Bats) 
PLoS ONE  2013;8(5):e64808.
The study of rabies virus infection in bats can be challenging due to quarantine requirements, husbandry concerns, genetic differences among animals, and lack of medical history. To date, all rabies virus (RABV) studies in bats have been performed in wild caught animals. Determining the RABV exposure history of a wild caught bat based on the presence or absence of viral neutralizing antibodies (VNA) may be misleading. Previous studies have demonstrated that the presence of VNA following natural or experimental inoculation is often ephemeral. With this knowledge, it is difficult to determine if a seronegative, wild caught bat has been previously exposed to RABV. The influence of prior rabies exposure in healthy, wild caught bats is unknown. To investigate the pathogenesis of RABV infection in bats born in captivity (naïve bats), naïve bats were inoculated intramuscularly with one of two Eptesicus fuscus rabies virus variants, EfV1 or EfV2. To determine the host response to a heterologous RABV, a separate group of naïve bats were inoculated with a Lasionycteris noctivagans RABV (LnV1). Six months following the first inoculation, all bats were challenged with EfV2. Our results indicate that naïve bats may have some level of innate resistance to intramuscular RABV inoculation. Additionally, naïve bats inoculated with the LnV demonstrated the lowest clinical infection rate of all groups. However, primary inoculation with EfV1 or LnV did not appear to be protective against a challenge with the more pathogenic EfV2.
PMCID: PMC3669413  PMID: 23741396
20.  Effects of sunlight on behavior and 25-hydroxyvitamin D levels in two species of Old World fruit bats 
Dermato-endocrinology  2013;5(1):192-198.
It has long been accepted that most vertebrate animals meet their vitamin D requirements from exposure of skin to UV-B (UV-B) radiation. Many factors affect this endogenous synthesis of vitamin D, including season, latitude, time of day, age, presence of hair, and degree of skin pigmentation. Most bats roost in dark places by day and forage at night, and thus have little or no potential for sunlight exposure. Notwithstanding, some tropical species are diurnal and are known to roost in the canopy of trees where they may be exposed to sunlight for up to 12 h each day. In this study, two species of captive tropical bats (both species are active at night but one, Rousettus aegyptiacus, roosts in caves, tombs, and buildings, whereas the other, Pteropus hypomelanus, roosts in trees) were evaluated for their ability to endogenously synthesize vitamin D. Following timed periods of sunlight exposure, blood plasma was analyzed using a competitive protein binding assay (CPBA) to determine concentrations of 25-hydroxyvitamin D [25(OH)D], the major circulating vitamin D metabolite. The ability to photoconvert provitamin D (7-dehydrocholesterol, 7-DHC) in the sub-tropical winter was determined using sunlight exposed borosilicate samples of 7-DHC in hourly increments. Finally, both species were evaluated in their preference for a roost site by the release of individuals into sunlight or shade in timed trials.
Our results support the hypotheses: (1) when exposed to natural sunlight, both species exhibited an ability to endogenously synthesize vitamin D, although significant differences were found between the two, (2) photoconversion of 7-DHC to previtamin D3 is possible during the mid-day hours of a sub-tropical winter day and (3) captive, cave roosting R. aegyptiacus will choose shaded roost sites while captive P. hypomelanus will show no preference for either shade or sun.
PMCID: PMC3897589  PMID: 24494054
bats; calcium; Chiroptera; sunlight; UV-B radiation; vitamin D
21.  Bartonella spp. in Fruit Bats and Blood-Feeding Ectoparasites in Madagascar 
PLoS Neglected Tropical Diseases  2015;9(2):e0003532.
We captured, ectoparasite-combed, and blood-sampled cave-roosting Madagascan fruit bats (Eidolon dupreanum) and tree-roosting Madagascan flying foxes (Pteropus rufus) in four single-species roosts within a sympatric geographic foraging range for these species in central Madagascar. We describe infection with novel Bartonella spp. in sampled Eidolon dupreanum and associated bat flies (Cyclopodia dubia), which nest close to or within major known Bartonella lineages; simultaneously, we report the absence of Bartonella spp. in Thaumapsylla sp. fleas collected from these same bats. This represents the first documented finding of Bartonella infection in these species of bat and bat fly, as well as a new geographic record for Thaumapsylla sp. We further relate the absence of both Bartonella spp. and ectoparasites in sympatrically sampled Pteropus rufus, thus suggestive of a potential role for bat flies in Bartonella spp. transmission. These findings shed light on transmission ecology of bat-borne Bartonella spp., recently demonstrated as a potentially zoonotic pathogen.
Author Summary
Bartonella spp. are bacteria that inhabit the red blood cells of both human and animal hosts. Among humans, Bartonella spp. are known to cause several febrile illnesses, including Carrion’s disease (Bartonella bacilliformis), trench fever (Bartonella quintana), and cat scratch fever (Bartonella henselae), all of which are transmitted via arthropod vectors—respectively sand flies, lice, and fleas. Bats are known to host multiple Bartonella spp., including some capable of infecting humans. Some bat species are also known to host obligate ectoparasites known as bat flies (Diptera: Hippoboscoidea), which also sometimes support Bartonella spp. infections. The role of bat flies and other bat ectoparasites as vectors for Bartonella spp. transmission has been suggested, but not fully explored. We demonstrate Bartonella spp. infection in one species of Madagascar fruit bat, which hosts bat flies, simultaneously with the absence of Bartonella in a fruit bat species of overlapping range that appears not to support these ectoparasites. In light of ongoing trends of zoonotic emergence of human diseases from bat reservoirs, further understanding of the transmission dynamics of bat-borne pathogens is paramount.
PMCID: PMC4337899  PMID: 25706653
22.  Diseases and Causes of Death in European Bats: Dynamics in Disease Susceptibility and Infection Rates 
PLoS ONE  2011;6(12):e29773.
Bats receive increasing attention in infectious disease studies, because of their well recognized status as reservoir species for various infectious agents. This is even more important, as bats with their capability of long distance dispersal and complex social structures are unique in the way microbes could be spread by these mammalian species. Nevertheless, infection studies in bats are predominantly limited to the identification of specific pathogens presenting a potential health threat to humans. But the impact of infectious agents on the individual host and their importance on bat mortality is largely unknown and has been neglected in most studies published to date.
Methodology/Principal Findings
Between 2002 and 2009, 486 deceased bats of 19 European species (family Vespertilionidae) were collected in different geographic regions in Germany. Most animals represented individual cases that have been incidentally found close to roosting sites or near human habitation in urban and urban-like environments. The bat carcasses were subjected to a post-mortem examination and investigated histo-pathologically, bacteriologically and virologically. Trauma and disease represented the most important causes of death in these bats. Comparative analysis of pathological findings and microbiological results show that microbial agents indeed have an impact on bats succumbing to infectious diseases, with fatal bacterial, viral and parasitic infections found in at least 12% of the bats investigated.
Our data demonstrate the importance of diseases and infectious agents as cause of death in European bat species. The clear seasonal and individual variations in disease prevalence and infection rates indicate that maternity colonies are more susceptible to infectious agents, underlining the possible important role of host physiology, immunity and roosting behavior as risk factors for infection of bats.
PMCID: PMC3247292  PMID: 22216354
23.  Sympatric Woodland Myotis Bats Form Tight-Knit Social Groups with Exclusive Roost Home Ranges 
PLoS ONE  2014;9(10):e112225.
The structuring of wild animal populations can influence population dynamics, disease spread, and information transfer. Social network analysis potentially offers insights into these processes but is rarely, if ever, used to investigate more than one species in a community. We therefore compared the social, temporal and spatial networks of sympatric Myotis bats (M. nattereri (Natterer's bats) and M. daubentonii (Daubenton's bats)), and asked: (1) are there long-lasting social associations within species? (2) do the ranges occupied by roosting social groups overlap within or between species? (3) are M. daubentonii bachelor colonies excluded from roosting in areas used by maternity groups?
Using data on 490 ringed M. nattereri and 978 M. daubentonii from 379 colonies, we found that both species formed stable social groups encompassing multiple colonies. M. nattereri formed 11 mixed-sex social groups with few (4.3%) inter-group associations. Approximately half of all M. nattereri were associated with the same individuals when recaptured, with many associations being long-term (>100 days). In contrast, M. daubentonii were sexually segregated; only a quarter of pairs were associated at recapture after a few days, and inter-sex associations were not long-lasting. Social groups of M. nattereri and female M. daubentonii had small roost home ranges (mean 0.2 km2 in each case). Intra-specific overlap was low, but inter-specific overlap was high, suggesting territoriality within but not between species. M. daubentonii bachelor colonies did not appear to be excluded from roosting areas used by females.
Our data suggest marked species- and sex-specific patterns of disease and information transmission are likely between bats of the same genus despite sharing a common habitat. The clear partitioning of the woodland amongst social groups, and their apparent reliance on small patches of habitat for roosting, means that localised woodland management may be more important to bat conservation than previously recognised.
PMCID: PMC4214762  PMID: 25356770
24.  Roosting Ecology and the Evolution of Pelage Markings in Bats 
PLoS ONE  2011;6(10):e25845.
Multiple lineages of bats have evolved striking facial and body pelage makings, including spots, stripes and countershading. Although researchers have hypothesized that these markings mainly evolved for crypsis, this idea has never been tested in a quantitative and comparative context. We present the first comparative study integrating data on roosting ecology (roost type and colony size) and pelage coloration patterns across bats, and explore the hypothesis that the evolution of bat pelage markings is associated with roosting ecologies that benefit from crypsis. We find that lineages that roost in the vegetation have evolved pelage markings, especially stripes and neck collars, which may function in crypsis through disruptive coloration and a type of countershading that might be unique to bats. We also demonstrate that lineages that live in larger colonies and are larger in size tend not to have pelage markings, possibly because of reduced predation pressures due to the predator dilution effect and a lower number of potential predators. Although social functions for pelage color patterns are also possible, our work provides strong support for the idea that roosting ecology has driven the evolution of pelage markings in bats.
PMCID: PMC3185059  PMID: 21991371
25.  Long-Distance and Frequent Movements of the Flying-Fox Pteropus poliocephalus: Implications for Management 
PLoS ONE  2012;7(8):e42532.
Flying-foxes (Pteropodidae) are large bats capable of long-distance flight. Many species are threatened; some are considered pests. Effective conservation and management of flying-foxes are constrained by lack of knowledge of their ecology, especially of movement patterns over large spatial scales. Using satellite telemetry, we quantified long-distance movements of the grey-headed flying-fox Pteropus poliocephalus among roost sites in eastern Australia. Fourteen adult males were tracked for 2–40 weeks (mean 25 weeks). Collectively, these individuals utilised 77 roost sites in an area spanning 1,075 km by 128 km. Movement patterns varied greatly between individuals, with some travelling long distances. Five individuals travelled cumulative distances >1,000 km over the study period. Five individuals showed net displacements >300 km during one month, including one movement of 500 km within 48 hours. Seasonal movements were consistent with facultative latitudinal migration in part of the population. Flying-foxes shifted roost sites frequently: 64% of roost visits lasted <5 consecutive days, although some individuals remained at one roost for several months. Modal 2-day distances between consecutive roosts were 21–50 km (mean 45 km, range 3–166 km). Of 13 individuals tracked for >12 weeks, 10 moved >100 km in one or more weeks. Median cumulative displacement distances over 1, 10 and 30 weeks were 0 km, 260 km and 821 km, respectively. On average, over increasing time-periods, one additional roost site was visited for each additional 100 km travelled. These findings explain why culling and relocation attempts have had limited success in resolving human-bat conflicts in Australia. Flying-foxes are highly mobile between camps and regularly travel long distances. Consequently, local control actions are likely to have only temporary effects on local flying-fox populations. Developing alternative methods to manage these conflicts remains an important challenge that should be informed by a better understanding of the species’ movement patterns.
PMCID: PMC3411823  PMID: 22880021

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