Vampire Bat Research Articles

Population of hematophagous bats in the Andradina region, São Paulo: roost and control characterization

The present study quantified Desmodus rotundus population and characterized their roosts in the Andradina microregion, Sao Paulo, Brazil, in 2010 and 2012, determining the effect of bat control measures on roost numbers and types and their population. From April to June 2010, professionals from the Agriculture and Livestock Defense Coordination of the State of Sao Paulo responsible for the rabies control that consists of capturing and treating vampire bats with a vampiricide paste based on Warfarin 2%, inspected 50 bat roosts registered in 12 municipalities in the Andradina microregion, northwestern Sao Paulo. In September 2012, 31 of these roosts were again surveyed by the authors of this study. The vast majority (92% and 96% in 2010 and 2012, respectively) of the roosts were characterized as artificial, e.g., abandoned houses and warehouses, house attics, culverts under highways, deactivated wells and mills, bridges, disused housings, and barns. The only natural roosts found were tree hollows. The number of roosts and the bat population in roosts decreased drastically after the measures for direct control of hematophagous bats were performed, especially the number of maternity colonies, indicating that the direct selective method had a strong impact on reducing these populations.

Retention and losses of ultraviolet-sensitive visual pigments in bats

Ultraviolet (UV)-sensitive visual pigment and its corresponding ability for UV vision was retained in early mammals from their common ancestry with sauropsids. Subsequently, UV-sensitive pigments, encoded by the short wavelength-sensitive 1 (SWS1) opsin gene, were converted to violet sensitivity or have lost function in multiple lineages during the diversification of mammals. However, many mammalian species, including most bats, are suggested to retain a UV-sensitive pigment. Notably, some cave-dwelling fruit bats and high duty cycle echolocating bats have lost their SWS1 genes, which are proposed to be due to their roosting ecology and as a sensory trade-off between vision and echolocation, respectively. Here, we sequenced SWS1 genes from ecologically diverse bats and found that this gene is also non-functional in both common vampire bat (Desmodus rotundus) and white-winged vampire bat (Diaemus youngi). Apart from species with pesudogenes, our evolutionary and functional studies demonstrate that the SWS1 pigment of bats are UV-sensitive and well-conserved since their common ancestor, suggesting an important role across major ecological types. Given the constrained function of SWS1 pigments in these bats, why some other species, such as vampire bats, have lost this gene is even more interesting and needs further investigation.

The impact of paralytic bovine rabies transmitted by vampire bats in Latin America and the Caribbean.

The effective control of dog rabies in Latin America is justifiably seen as a major success in the struggle to limit this devastating zoonosis. However, rabies remains a problem, due to the presence of the virus in bat populations throughout the region, including vampire bats. Vampire bats obtain nutrition exclusively through consuming blood by biting mammals and birds. This makes the species a highly efficient vector of the rabies virus, responsible for sporadic outbreaks of rabies in human populations and numerous cases of rabies in livestock. This, in turn, causes economic losses to the farming industry in countries throughout the region. For over four decades, efforts to control rabies have been directed at controlling the reservoir species and vaccinating cattle. However, this approach has not eliminated rabies in livestock. A major barrier to innovation in vampire rabies control is a lack of consistent surveillance to establish the extent of the problem. This precludes any calculation of its cost to the economy or the cost of potential solutions, such as vaccinating livestock. This paper outlines the problem of livestock rabies in Latin America and considers factors that influence the economic cost of potential solutions to this continuing challenge to human and livestock health.

GENETIC RELATEDNESS OF Desmodus rotundus FROM NORTHERN URUGUAY WITH POPULATIONS FROM THE REMAINDER OF ITS DISTRIBUTION RANGE

The common vampire bat (Desmodus rotundus), which is distributed across most of the Neotropical region, is a reservoir of the rabies virus. In Uruguay, there have been recent reports of paralytic rabies in cattle transmitted by the common vampire bat. We sequenced the cytochrome b gene of five bats from northern Uruguay. All five DNA sequences were identical and grouped with a southern Atlantic Forest clade, suggesting recent dispersal from nearby Brazil, as revealed in phylogeographic diffusion analysis.

Detection of rabies virus in organs unrelated to the central nervous system of experimentally-inoculated vampire bats

The aim of this research was to detect rabies virus in peripheral tissues in captive vampires. Vampire bats were inoculated with 106 MICLD50 of homologous rabies virus. Bats displayed clinical signs of rabies beginning on d 8 until the 19th d post-inoculation (pi). Rabies virus antigens were found in the brain of all rabid bats. Viral RNA was detected in brain, salivary gland and tongue tissue by RT-PCR and nested PCR (nPCR). Viral genome was also detected in organs unrelated to the central nervous system. Rabies virus was not detected in saliva nor documented from any tissues without occurrence of viral antigens in the brain. Host humoral response was most pronounced via the induction of viral neutralizing antibodies (VNA) from d 8 to 20 pi, having a peak at d 14 with 0.9 IU. Antibody levels were variable, but tended to remain high after inoculation, showing significant differences to the negative control group (P=0.001). This research is one of the few recent studies focused upon Desmodus rotundus and contributes to the basic knowledge of rabies virus pathogenesis, which is required for an understanding of perpetuation in a major viral reservoir in Latin America.

Septicemia due to Streptococcus dysgalactiae subspecies dysgalactiae in vampire bats (Desmodus rotundus)

Beta-hemolytic Streptococcus dysgalactiae is a well-known pathogen for a wide range of animals and humans. Two subspecies are recognized: (i) equisimilis, associated to disease in horses and humans, and (ii) dysgalactiae mainly isolated from animal illness with only a few humans’ cases. This study describes the isolation and characterization of Streptococcus dysgalactiae subsp. dysgalactiae (SDSD) from vampire bats, maintained in captivity for research proposes. Animals presented neurologic, respiratory and gastroenteric symptoms and sudden death. Beta-hemolytic Gram-positive cocci were isolated in blood agar plates and further characterized as Lancefield group C. All isolates were identified as S. dysgalactiae by matrix-assisted laser desorption/ionization-time of flight (MALDI-TOF) mass spectrometry and subspecies dysgalactiae was confirmed by 16S rRNA sequencing and phylogenetic analysis. Genotyping through SE-ALFP resulted in three profiles (A1–A3) with one bat being infected by profiles A1 and A3. This is the first report of SDSD causing illness in bats and especially in Desmodus rotundus species.

Detection of Bartonella species, including Candidatus Bartonella ovis sp. nov, in ruminants from Mexico and lack of evidence of Bartonella DNA in saliva of common vampire bats (Desmodus rotundus) predating on them

Bartonella spp. have been identified in many bat species worldwide, including the zoonotic species, Candidatus Bartonella mayotimonensis. The common vampire bat (Desmodus rotundus) preys preferentially on livestock in Latin America and is frequently infected with Bartonella spp. To determine the potential role of D. rotundus in transmitting Bartonella to livestock, common vampire bats and bat-bitten domestic ruminants from Mexico were tested for Bartonella infection by blood culture or conventional PCR. Furthermore, to explore the possibility of bite transmission during blood feeding, saliva swabs from 35 D. rotundus known to be either Bartonella bacteremic (N = 17) or blood culture negative (N = 18) were tested by PCR to detect the presence of Bartonella DNA. Twenty (17.1%) of 117 sheep and 16 (34.8%) of 46 cattle were Bartonella bacteremic by PCR testing. However, none of them were infected with Bartonella strains previously isolated from vampire bats and none of the 35 D. rotundus saliva swabs tested were PCR positive for Bartonella. All but two animals among those which were Bartonella culture and/or PCR positive, were infected with either B. bovis (cattle) or B. melophagi (sheep). Two sheep were infected by a possible new species, Candidatus Bartonella ovis, being phylogenetically closer to B. bovis than B. melophagi. This study does not support the role of D. rotundus as a reservoir of Bartonella species infecting livestock, which could be transmitted via bite and blood feeding and therefore suggest limited risk of zoonotic transmission of Bartonella from common vampire bats to humans.

In Cold Blood: Compositional Bias and Positive Selection Drive the High Evolutionary Rate of Vampire Bats Mitochondrial Genomes.

Mitochondrial genomes of animals have long been considered to evolve under the action of purifying selection. Nevertheless, there is increasing evidence that they can also undergo episodes of positive selection in response to shifts in physiological or environmental demands. Vampire bats experienced such a shift, as they are the only mammals feeding exclusively on blood and possessing anatomical adaptations to deal with the associated physiological requirements (e.g., ingestion of high amounts of liquid water and iron). We sequenced eight new chiropteran mitogenomes including two species of vampire bats, five representatives of other lineages of phyllostomids and one close outgroup. Conducting detailed comparative mitogenomic analyses, we found evidence for accelerated evolutionary rates at the nucleotide and amino acid levels in vampires. Moreover, the mitogenomes of vampire bats are characterized by an increased cytosine (C) content mirrored by a decrease in thymine (T) compared with other chiropterans. Proteins encoded by the vampire bat mitogenomes also exhibit a significant increase in threonine (Thr) and slight reductions in frequency of the hydrophobic residues isoleucine (Ile), valine (Val), methionine (Met), and phenylalanine (Phe). We show that these peculiar substitution patterns can be explained by the co-occurrence of both neutral (mutational bias) and adaptive (positive selection) processes. We propose that vampire bat mitogenomes may have been impacted by selection on mitochondrial proteins to accommodate the metabolism and nutritional qualities of blood meals.

Natural infection of Neotropical bats with hantavirus in Brazil

Bats (Order: Chiroptera) harbor a high diversity of emerging pathogens presumably because their ability to fly and social behavior favor the maintenance, evolution, and dissemination of these pathogens. Until 2012, there was only one report of the presence of Hantavirus in bats. Historically, it was thought that these viruses were harbored primarily by rodent and insectivore small mammals. Recently, new species of hantaviruses have been identified in bats from Africa and Asia continents expanding the potential reservoirs and range of these viruses. To assess the potential of Neotropical bats as hosts for hantaviruses and its transmission dynamics in nature, we tested 53 bats for active hantaviral infection from specimens collected in Southeastern Brazil. Part of the hantaviral S segment was amplified from the frugivorous Carollia perspicillata and the common vampire bat Desmodus rotundus. DNA sequencing showed high similarity with the genome of Araraquara orthohantavirus (ARQV), which belongs to one of the more lethal hantavirus clades (Andesorthohantavirus). ARQV-like infection was detected in the blood, urine, and organs of D. rotundus. Therefore, we describe a systemic infection in Neotropical bats by a human pathogenic Hantavirus. We also propose here a schematic transmission dynamics of hantavirus in the study region. Our results give insights to new, under-appreciated questions that need to be addressed in future studies to clarify hantavirus transmission in nature and avoid hantavirus outbreaks.

A method for rapid testing of social learning in vampire bats

Designing experiments on social learning using an untested behaviour or species requires baseline knowledge of how the animals will perform. We conducted a pilot study of a procedure for rapidly testing social learning in the highly social common vampire bat (Desmodus rotundus) using a simple maze. To create demonstrators, we allowed captive bats to learn to exit a three-dimensional maze, which reunited them with their colony as a reward. We then filmed naive bats in the same maze, comparing their ability to exit the maze before, during and after the addition of a trained demonstrator. The presence of a demonstrator increased the exit rates of naive bats, presumably by attracting the attention of the naive bats to the maze exit. Four of the five naive bats that exited in the presence of a demonstrator retained the ability to exit without the demonstrator. No naive bat exited during trials without a potential demonstrator present. This experimental procedure appears to be a promising approach for efficient tests of social learning in vampire bats because maze difficulty can be manipulated to adjust learning rates and each trial requires only 15 min.

An immune challenge reduces social grooming in vampire bats

Social interactions affect the transmission of many pathogens, but infections often induce sickness behaviours that alter those interactions. Vampire bats are highly mobile and social, engaging in frequent allogrooming, which is likely to facilitate pathogen spread. Sickness behaviour is known to reduce social associations, but the effect on physical interactions between associated individuals, such as grooming, is less understood. Here, we tested the effects of induced sickness behaviour on allogrooming in vampire bats, while holding association between individuals in groups constant. To experimentally induce sickness behaviour, we used injections of lipopolysaccharide (LPS) and saline controls in 13 female common vampire bats, Desmodus rotundus, housed in stable groups of two to four adult bats. LPS injection induced an immune response that mimicked illness. Circulating leukocytes and neutrophil:lymphocyte ratios increased, while body mass and activity decreased. While LPS-injected bats did not receive less grooming from their group mates, they dramatically reduced the amount that they groomed their partners. This reduction in social interactions illustrates that sickness behaviour can potentially change transmission rates by altering directed behaviours, even under conditions of constant close proximity. The ability to manipulate social behaviours under controlled conditions should also prove useful for experiments attempting to test mechanisms underlying cooperation.

Using DNA metabarcoding for simultaneous inference of common vampire bat diet and population structure.

Metabarcoding diet analysis has become a valuable tool in animal ecology; however, co‐amplified predator sequences are not generally used for anything other than to validate predator identity. Exemplified by the common vampire bat, we demonstrate the use of metabarcoding to infer predator population structure alongside diet assessments. Growing populations of common vampire bats impact human, livestock and wildlife health in Latin America through transmission of pathogens, such as lethal rabies viruses. Techniques to determine large‐scale variation in vampire bat diet and bat population structure would empower locality‐ and species‐specific projections of disease transmission risks. However, previously used methods are not cost‐effective and efficient for large‐scale applications. Using bloodmeal and faecal samples from common vampire bats from coastal, Andean and Amazonian regions of Peru, we showcase metabarcoding as a scalable tool to assess vampire bat population structure and feeding preferences. Dietary metabarcoding was highly effective, detecting vertebrate prey in 93.2% of the samples. Bats predominantly preyed on domestic animals, but fed on tapirs at one Amazonian site. In addition, we identified arthropods in 9.3% of samples, likely reflecting consumption of ectoparasites. Using the same data, we document mitochondrial geographic population structure in the common vampire bat in Peru. Such simultaneous inference of vampire bat diet and population structure can enable new insights into the interplay between vampire bat ecology and disease transmission risks. Importantly, the methodology can be incorporated into metabarcoding diet studies of other animals to couple information on diet and population structure.

Younger vampire bats (Desmodus rotundus) are more likely than adults to explore novel objects.

The effects of age on neophobia and exploration are best described in birds and primates, and broader comparisons require reports from other taxa. Here we present data showing age-dependent exploration in a long-lived social species, the common vampire bat (Desmodus rotundus). A previous study found that vampire bats regurgitated food to partners trapped in a cage. Interestingly, while only a few adult bats visited the trapped bat, in every trial all or most of the eight young males in the colony would visit the trapped bat without feeding it. To test whether this behavioral difference resulted from age class differences in exploration, we compared responses of the bats to a trapped conspecific versus an inanimate novel object. Some adults and young showed interest in trapped conspecifics, but only the young males explored the novel objects. Additional novel object tests in a second captive colony showed that higher rates of novel object exploration were shown by young of both sexes. Our results corroborate past findings from other mammals and birds that age predicts exploration. If age-dependent exploration is indeed adaptive, then the role of age as a predictor of exploration tendency should depend on species-specific life history traits. Finally, because younger vampire bats also appear to have higher exposure to pathogens such as rabies virus, there may be implications for pathogen transmission if younger and more exploratory vampire bats are more likely to feed on novel hosts.

A potential robust antiviral defense state in the common vampire bat: Expression, induction and molecular characterization of the three interferon-stimulated genes -OAS1, ADAR1 and PKR

Bats are known to harbor many zoonotic viruses, some of which are pathogenic to other mammals while they seem to be harmless in bats. As the interferon (IFN) response represents the first line of defense against viral infections in mammals, it is hypothesized that activation of the IFN system is one of the mechanisms enabling bats to co-exist with viruses. We have previously reported induction of type I IFN in a cell line from the common vampire bat, Desmodus rotundus, upon polyinosinic:polycytidylic acid (poly(I:C)) stimulation. To deepen our knowledge on D. rotundus’ IFN-I antiviral response, we molecularly characterized three interferon-stimulated genes (ISGs), OAS1, PKR and ADAR1, closely implicated in the IFN-I antiviral response, and tested their functionality in our cellular model. We first found that D. rotundus encoded two OAS1 paralogs, OAS1a and OAS1b, and that the functional domains of the four ISGs characterized were highly conserved with those of other mammals. Despite their significant transcription level in the absence of stimulation, the transcription of the four ISGs characterized was enhanced by poly(I:C). In addition, the transcription of OAS1a and OAS1b appears to be differentially regulated. These findings demonstrate an active ISG antiviral response in D. rotundus in which OAS1b may play an important role.

Filling gaps in the distribution of the white-winged vampire bat, Diaemus youngii (Phyllostomidae, Desmodontinae): new records for southern Amazonia

ABSTRACT Bats of the subfamily Desmodontinae are the only hematophagous mammals, represented by three species. Among them, Diaemus youngii has the fewest records in Brazil, being poorly known demographically and ecologically. We report the first record of D. youngii for Mato Grosso state, in central-western Brazil, and provide additional records for the states of Rondônia and Tocantins, in northern Brazil, extending the known distribution of D. youngii in the southern Amazon region.

Iron storage disease (hemochromatosis) and hepcidin response to iron load in two species of pteropodid fruit bats relative to the common vampire bat.

Hepcidin is the key regulator of iron homeostasis in the body. Iron storage disease (hemochromatosis) is a frequent cause of liver disease and mortality in captive Egyptian fruit bats (Rousettus aegyptiacus), but reasons underlying this condition are unknown. Hereditary hemochromatosis in humans is due to deficiency of hepcidin or resistance to the action of hepcidin. Here, we investigated the role of hepcidin in iron metabolism in one species of pteropodid bat that is prone to iron storage disease [Egyptian fruit bat (with and without hemochromatosis)], one species of pteropodid bat where iron storage disease is rare [straw-colored fruit bat (Eidolon helvum)], and one species of bat with a natural diet very high in iron, in which iron storage disease is not reported [common vampire bat (Desmodus rotundus)]. Iron challenge via intramuscular injection of iron dextran resulted in significantly increased liver iron content and histologic iron scores in all three species, and increased plasma iron in Egyptian fruit bats and straw-colored fruit bats. Hepcidin mRNA expression increased in response to iron administration in healthy Egyptian fruit bats and common vampire bats, but not in straw-colored fruit bats or Egyptian fruit bats with hemochromatosis. Hepcidin gene expression significantly correlated with liver iron content in Egyptian fruit bats and common vampire bats, and with transferrin saturation and plasma ferritin concentration in Egyptian fruit bats. Induction of hepcidin gene expression in response to iron challenge is absent in straw-colored fruit bats and in Egyptian fruit bats with hemochromatosis and, relative to common vampire bats and healthy humans, is low in Egyptain fruit bats without hemochromatosis. Limited hepcidin response to iron challenge may contribute to the increased susceptibility of Egyptian fruit bats to iron storage disease.

Extended-spectrum beta-lactamase-producing Escherichia coli in common vampire bats Desmodus rotundus and livestock in Peru.

SummaryAntibiotic resistance mediated by bacterial production of extended‐spectrum beta‐lactamase (ESBL) is a global threat to public health. ESBL resistance is most commonly hospital‐acquired; however, infections acquired outside of hospital settings have raised concerns over the role of livestock and wildlife in the zoonotic spread of ESBL‐producing bacteria. Only limited data are available on the circulation of ESBL‐producing bacteria in animals. Here, we report ESBL‐producing Escherichia coli in wild common vampire bats Desmodus rotundus and livestock near Lima, Peru. Molecular analyses revealed that most of this resistance resulted from the expression of bla CTX‐M‐15 genes carried by plasmids, which are disseminating worldwide in hospital settings and have also been observed in healthy children of Peru. Multilocus sequence typing showed a diverse pool of E. coli strains carrying this resistance that were not always host species‐specific, suggesting sharing of strains between species or infection from a common source. This study shows widespread ESBL resistance in wild and domestic animals, supporting animal communities as a potential source of resistance. Future work is needed to elucidate the role of bats in the dissemination of antibiotic‐resistant strains of public health importance and to understand the origin of the observed resistance.

Molecular Detection ofBartonellaSpecies in Blood-Feeding Bat Flies from Mexico

Bartonellae are emerging blood-borne bacteria that have been recovered from a wide range of mammalian species and arthropod vectors around the world. Bats are now recognized as a potential wildlife reservoir for a diverse number of Bartonella species, including the zoonotic Candidatus B. mayotimonensis. These bat-borne Bartonella species have also been detected in the obligate ectoparasites of bats, such as blood-feeding flies, which could transmit these bacteria within bat populations. To better understand this potential for transmission, we investigated the relatedness between Bartonella detected or isolated from bat hosts sampled in Mexico and their ectoparasites. Bartonella spp. were identified in bat flies collected on two bat species, with the highest prevalence in Trichobius parasiticus and Strebla wiedemanni collected from common vampire bats (Desmodus rotundus). When comparing Bartonella sequences from a fragment of the citrate synthase gene (gltA), vector-associated strains were diverse and generally close to, but distinct from, those recovered from their bacteremic bat hosts in Mexico. Complete Bartonella sequence concordance was observed in only one bat-vector pair. The diversity of Bartonella strains in bat flies reflects the frequent host switch by bat flies, as they usually do not live permanently on their bat host. It may also suggest a possible endosymbiotic relationship with these vectors for some of the Bartonella species carried by bat flies, whereas others could have a mammalian host.

Livestock abundance predicts vampire bat demography, immune profiles and bacterial infection risk.

Human activities create novel food resources that can alter wildlife–pathogen interactions. If resources amplify or dampen, pathogen transmission probably depends on both host ecology and pathogen biology, but studies that measure responses to provisioning across both scales are rare. We tested these relationships with a 4-year study of 369 common vampire bats across 10 sites in Peru and Belize that differ in the abundance of livestock, an important anthropogenic food source. We quantified innate and adaptive immunity from bats and assessed infection with two common bacteria. We predicted that abundant livestock could reduce starvation and foraging effort, allowing for greater investments in immunity. Bats from high-livestock sites had higher microbicidal activity and proportions of neutrophils but lower immunoglobulin G and proportions of lymphocytes, suggesting more investment in innate relative to adaptive immunity and either greater chronic stress or pathogen exposure. This relationship was most pronounced in reproductive bats, which were also more common in high-livestock sites, suggesting feedbacks between demographic correlates of provisioning and immunity. Infection with both Bartonella and haemoplasmas were correlated with similar immune profiles, and both pathogens tended to be less prevalent in high-livestock sites, although effects were weaker for haemoplasmas. These differing responses to provisioning might therefore reflect distinct transmission processes. Predicting how provisioning alters host–pathogen interactions requires considering how both within-host processes and transmission modes respond to resource shifts.This article is part of the theme issue ‘Anthropogenic resource subsidies and host–parasite dynamics in wildlife’.

Comparative genomics: Blood, guts and vampire bats.

Comparative genomics: Blood, guts and vampire bats.