Native Bats Research Articles

Functional characterization of a cystatin A from the bat Myotis davidii

Myotis davidii cystatin A (MdCSTA), a stefin A-like from the Chinese native bat species M. davidii, was expressed as a recombinant protein and functionally characterized as a strong inhibitor of the cysteine proteases papain, human cathepsins L and B and the tick cathepsin L-like BmCL1. Despite the highly conserved amino acid sequences among stefins A from different vertebrates, MdCSTA presents a Methionine-2 residue at the N-terminal region and the second binding loop (pos 73–79) that differs from human stefin A (HsCSTA) and might be related to the lower inhibition constant (Ki) value presented by this inhibitor in comparison to human stefin A inhibition to cathepsin B. Therefore, to investigate the importance of these variable regions in cathepsin B inhibition, recombinant stefins A MdCSTA and HsCSTA containing mutations at the second amino acid residue and second binding loop were expressed and evaluated in kinetic assays. Enzymatic inhibition assays with cathepsin B revealed that switching the amino acid residues at position 2 and second binding loop region between bat and human CSTAs improved the HsCSTA's and reduced MdCSTA's inhibitory activity. Additionally, molecular docking analysis estimated lower energy values for the complex between MdCSTA-cathepsin B, in comparison to human CSTA-cathepsin B, while the mutants presented intermediate values, suggesting that other regions might contribute to the higher inhibitory activity against cathepsin B by MdCSTA. In conclusion, MdCSTA, the first bat's stefin A-like inhibitor to be functionally characterized, presented a higher inhibitory activity against cathepsin B in comparison to the human inhibitor, which is partially related to the glutamine-rich second binding loop and Met-2. Further structural analysis should be performed to elucidate potential inhibitor effects on cysteine proteinases.

Impacts on Bats by a Supertyphoon vs. Ordinary Typhoons along a Habitat Urbanization Gradient

Two major human-caused threats to ecosystems are habitat modification and the increasing frequency and intensity of extreme weather events. To study the combined effect of these threats, the authors used acoustic monitoring of bats along a habitat modification gradient on the island of Okinawa, Japan. During the observation period, the island experienced numerous typhoons and one supertyphoon. Native bat species remained active even at high wind speeds (up to 30 m/s in some cases). Milder typhoons had no observable effect on bat populations, with activity levels fully recovering within a few hours or days. The super typhoon also did not seem to affect bats in fully or partially forested habitats but caused their local disappearance at the urban site, which they have not re-colonized three years after the event. Notably, bats that disappeared at the urban site were species roosting in well-protected places such as caves and concrete structures. In all cases, the biomass of small flying insects and the acoustic activity of insects recovered within days after extreme weather events. Thus, the striking difference between habitats in supertyphoon effects on bats cannot be explained by the super typhoon directly killing bats, destroying their roosting sites, or decreasing the abundance of their prey. The results underscore the importance of preserving natural habitats in areas particularly affected by changing climate and show that the survival of species and ecosystems during the numerous episodes of climate change in the Earth’s history does not necessarily mean their ability to survive the accelerating climate change of our time.

Genomic screening of 16 UK native bat species through conservationist networks uncovers coronaviruses with zoonotic potential

There has been limited characterisation of bat-borne coronaviruses in Europe. Here, we screened for coronaviruses in 48 faecal samples from 16 of the 17 bat species breeding in the UK, collected through a bat rehabilitation and conservationist network. We recovered nine complete genomes, including two novel coronavirus species, across six bat species: four alphacoronaviruses, a MERS-related betacoronavirus, and four closely related sarbecoviruses. We demonstrate that at least one of these sarbecoviruses can bind and use the human ACE2 receptor for infecting human cells, albeit suboptimally. Additionally, the spike proteins of these sarbecoviruses possess an R-A-K-Q motif, which lies only one nucleotide mutation away from a furin cleavage site (FCS) that enhances infectivity in other coronaviruses, including SARS-CoV-2. However, mutating this motif to an FCS does not enable spike cleavage. Overall, while UK sarbecoviruses would require further molecular adaptations to infect humans, their zoonotic risk warrants closer surveillance.

Environmental transmission of Pseudogymnoascus destructans to hibernating little brown bats

Pathogens with persistent environmental stages can have devastating effects on wildlife communities. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in bat populations of North America. In 2009, during the early stages of the WNS investigation and before molecular techniques had been developed to readily detect P. destructans in environmental samples, we initiated this study to assess whether P. destructans can persist in the hibernaculum environment in the absence of its conclusive bat host and cause infections in naive bats. We transferred little brown bats (Myotis lucifugus) from an unaffected winter colony in northwest Wisconsin to two P. destructans contaminated hibernacula in Vermont where native bats had been excluded. Infection with P. destructans was apparent on some bats within 8 weeks following the introduction of unexposed bats to these environments, and mortality from WNS was confirmed by histopathology at both sites 14 weeks following introduction. These results indicate that environmental exposure to P. destructans is sufficient to cause the infection and mortality associated with WNS in naive bats, which increases the probability of winter colony extirpation and complicates conservation efforts.

ROADWAY-ASSOCIATED CULVERTS MAY SERVE AS A TRANSMISSION CORRIDOR FOR PSEUDOGYMNOASCUS DESTRUCTANS AND WHITE-NOSE SYNDROME IN THE COASTAL PLAINS AND COASTAL REGION OF GEORGIA, USA.

White-nose syndrome (WNS) is a disease among hibernating North American bats caused by the psychrophilic fungus Pseudogymnoascus destructans. Since its discovery in New York state, US, in 2006, and as of 2020, WNS has rapidly spread to 34 American states and seven Canadian provinces, causing precipitous declines of native bat populations across North America. The rapid spread of this fungal pathogen has been facilitated by the social behavior of bats, as well as the ability of subterranean hibernacula to support a favorable environment for P. destructans, and is probably exacerbated by anthropogenic transmission events. Although many bat species roost in natural cave environments, bats also selectively use diverse structures for hibernacula. Certain areas of the US lack caves, forcing bats to select different winter roosting environments. Bats have been observed using roadway-associated structures, such as bridges and culverts, for roosting, especially in regions that lack natural cave environments. However, the potential for P. destructans transmission in such roadway-associated structures requires further investigation. Understanding potential pathogen transmission in these widely used anthropogenic structures is crucial to disease management and preventing further declines of imperiled bat populations. Our study investigated these structures as potential pathogen transmission corridors by surveying the use of these structures by Perimyotis subflavus and other susceptible bat populations and by measuring their temperature. The results suggest the environments of roadway-associated culverts are thermally conducive to the proliferation of P. destructans-even in regions with mild winters-and the development of WNS in susceptible bat populations. It is apparent these roadway-associated structures have the potential to spread P. destructans and exacerbate the effect of WNS on susceptible bat populations.

Novel diplochory: Native bats and non-native rats disperse seeds of an island tree

Many oceanic islands lacked mammalian seed predators until humans introduced rats (Rattus spp.). Introduced rats are considered major seed predators on the islands where they occur, but their capacity to assist native plant recruitment through secondary dispersal, or diplochory, is poorly known. We monitored fates of >1000 naturally- and artificially-dispersed diaspores of the coastal tree Pandanus tectorius, to assess potential effects of rats on seedling recruitment in Tonga (Polynesia) and to determine if diplochory (phase II dispersal) by invasive rats can enhance primary dispersal (phase I) achieved by native bats. Pandanus diaspores consist of multiple single-seeded fruits (drupes) fused into a “phalange" in which each seed is protected by a stony endocarp, and all endocarps are fused into a single, solid structure. Native bats (Pteropus tonganus) consumed the pulp of the diaspores and dispersed 61% of them away from the crown. Introduced rats (Rattus rattus, R. exulans), consumed pulp and seeds. Rats secondarily dispersed 39% of the phalanges bats dropped below trees, carrying most of them away from trees. The average phalange has 6–7 outer drupes around its circumference, surrounding 2–3 inner drupes. Rats removed seeds from 64% of outer drupes, but opened no inner drupes; therefore, phalanges typically retained at least one uneaten seed. Of these rat-handled phalanges, 69% produced at least one seedling, compared to 96% of unhandled phalanges. Overall, diplochory, the combined effect of phase I dispersal by bats and phase II dispersal by rats, increased the likelihood that a phalange would produce a seedling that was not beneath the parent crown by 34%, when compared to the effect of bats alone. Seedling recruitment is unlikely to be strongly reduced by rodent seed predators, since rats do not consume all seeds in a single diaspore, and losses from predation may be offset by rats assisting the “escape” of the diaspores dropped by bats underneath the fruiting crown.

First report of Trypanosoma dionisii (Trypanosomatidae) identified in Australia.

Trypanosomes are blood-borne parasites that can infect a variety of different vertebrates, including animals and humans. This study aims to broaden scientific knowledge about the presence and biodiversity of trypanosomes in Australian bats. Molecular and morphological analysis was performed on 86 blood samples collected from seven different species of microbats in Western Australia. Phylogenetic analysis on 18S rDNA and glycosomal glyceraldehyde phosphate dehydrogenase (gGAPDH) sequences identified Trypanosoma dionisii in five different Australian native species of microbats; Chalinolobus gouldii, Chalinolobus morio, Nyctophilus geoffroyi, Nyctophilus major and Scotorepens balstoni. In addition, two novels, genetically distinct T. dionisii genotypes were detected and named T. dionisii genotype Aus 1 and T. dionisii genotype Aus 2. Genotype Aus 2 was the most prevalent and infected 20.9% (18/86) of bats in the present study, while genotype Aus 1 was less prevalent and was identified in 5.8% (5/86) of Australian bats. Morphological analysis was conducted on trypomastigotes identified in blood films, with morphological parameters consistent with trypanosome species in the subgenus Schizotrypanum. This is the first report of T. dionisii in Australia and in Australian native bats, which further contributes to the global distribution of this cosmopolitan bat trypanosome.

Rediscovery of Van Hasselt’s Mouse-eared Bat Myotis hasseltii (Temminck, 1840) and its first genetic data from Hanoi, northern Vietnam

This paper presents the rediscovery of Van Hasselt’s Mouse-eared Bat Myotis hasseltii after nearly 50 years and its genetic data from Hanoi, northern Vietnam. In addition, a snapshot of the impacts of urbanization on the current distribution and conservation status of this native bat species in Hanoi is also provided.

Does the fungus causing white-nose syndrome pose a significant risk to Australian bats?

Abstract ContextPseudogymnoascus destructans is the fungus responsible for white-nose syndrome (WNS), which has killed millions of hibernating bats in North America, but also occurs in bats in Europe and China without causing large-scale population effects. This is likely to be due to differences in species susceptibility and behaviour, and environmental factors, such as temperature and humidity. Pseudogymnoascus destructans is currently believed to be absent from Australia. AimsTo ascertain the level of risk that white-nose syndrome poses for Australian bats. Methods This risk analysis examines the likelihood that P. destructans enters Australia, the likelihood of the fungus coming in contact with native bats on successful entry, and the potential consequences should this occur. Key results This risk assessment concluded that it is very likely to almost certain that P. destructans will enter Australia, and it is likely that bats will be exposed to the fungus over the next 10 years. Eight cave-dwelling bat species from southern Australia are the ones most likely to be affected. ConclusionsThe risk was assessed as medium for the critically endangered southern bent-winged bat (Miniopterus orianae bassanii), because any increase in mortality could affect its long-term survival. The risk to other species was deemed to range from low to very low, owing to their wider distribution, which extends beyond the P. destructans risk zone. Implications Although Australia’s milder climate may preclude the large mortality events seen in North America, the fungus could still significantly affect Australian bat populations, particularly bent-winged bats. Active surveillance is required to confirm Australia’s continuing WNS-free status, and to detect the presence of P. destructans should it enter the country. Although White-nose Syndrome Response Guidelines have been developed by Wildlife Health Australia to assist response agencies in the event of an incursion of WNS into bats in Australia, these guidelines would be strengthened by further research to characterise Australian cave temperatures and hibernating bat biology, such as length of torpor bouts and movement over winter. Risk-mitigation strategies should focus on education programs that target cavers, show-cave managers and tourists, particularly those who have visited regions where WNS is known to occur.

Identification of Probiotic Bacteria from the Cutaneous Microbiome of Endangered Tennessee Bats

Since its arrival in 2006, the fungal agent of White‐Nose Syndrome (WNS), Psuedogymnascus destructans (Pd), has rapidly spread across the eastern United States. As a result, millions of native bats have been killed. This fungal pathogen infects bats in cave systems during their hibernation, causing disruption of natural physiological processes. Notably, the affected species experience an increased frequency of arousal from hibernation, which causes them to consume more of their reserved energy, eventually causing the bat to die of starvation. WNS, which is capable of producing a near 100% mortality rate within the bat's roost during a given hibernation cycle, has been confirmed to infect nine bat species present in the Eastern United States, three of which are federally listed as endangered. The presence of Pd has also been observed on six additional bat species without causing diagnostic symptoms. To provide treatment for Pd, current options include the use of anti‐fungal and volatile compounds as well as naturally occurring probiotic bacteria. The primary objectives of this research are 1) to evaluate and determine if the resident cutaneous microbiome of bats displays anti‐fungal activity against this fungal pathogen, and 2) to identify key probiotic bacterial strains for future biocontrol assessment. Currently, 355 bacterial isolates have been isolated into pure culture from 78 bat skin swab samples. It has been determined that through the use of microbiological challenge assays of the bacterial isolates against Pd, that 111 cultures from bat skin exhibit production of diffusible organic compounds and metabolites that display anti‐fungal activity against Pd. An isolate from the Actinobacteria (genus Streptomyces) has been identified to produce volatile organic compounds that completely inhibit fungal growth. Identification of the bioactive compound(s) is under investigation.Support or Funding InformationSupport and funding were provided by the Tennessee Wildlife Resources Agency.This abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Chirosurveillance: The use of native bats to detect invasive agricultural pests

Invasive insect pests cost the agricultural industry billions of dollars annually in crop losses. Timely detection of pests is critical for management efficiency. Innovative pest detection strategies, such as environmental DNA (eDNA) techniques, combined with efficient predators, maximize sampling resolution across space and time and may improve surveillance. We tested the hypothesis that temperate insectivorous bats can be important sentinels of agricultural insect pest surveillance. Specifically, we used a new high-sensitivity molecular assay for invasive brown marmorated stink bugs (Halyomorpha halys) to examine the extent to which big brown bats (Eptesicus fuscus) detect agricultural pests in the landscape. We documented consistent seasonal predation of stink bugs by big brown bats. Importantly, bats detected brown marmorated stink bugs 3–4 weeks earlier than the current standard monitoring tool, blacklight traps, across all sites. We highlight here the previously unrecognized potential ecosystem service of bats as agents of pest surveillance (or chirosurveillance). Additional studies examining interactions between other bat and insect pest species, coupled with comparisons of detectability among various conventional monitoring methods, are needed to verify the patterns extracted from this study. Ultimately, robust economic analyses will be needed to assess the cost-effectiveness of chirosurveillance as a standard strategy for integrated pest management.

Two cases of bat pollination in Central America

Visits by bats of the family ,Phyllostomatidae (in the suborder Microchi­roptera) to the flowers of Durio zibethinus growing in Honduras and Mucuna andreana growing in Costa Rica are described and illustrated photographically. In Durio we have a case of flower-type which evolved in relation to visits from Megachiroptera in the Old World proving attractive to Microchiroptera which developed the flower-visiting habit in the New World. Hawkmoths also visit these flowers. Both kinds of visitor are capable of causing cross-pollination (which is necessary for fruit production by this species because it appears to be self-incompatible) . In Mucuna andreana , a native American vine demons­ trates a close adaptation to pollination by native bats; again a parallel to similar evolutionary development in the Old World.

Feeding and parasitism of adultStenoperlaspp. (Plecoptera: Eustheniidae) in New Zealand

AbstractThe adult diets of two species of stonefly,Stenoperla prasina(Newman, 1845) andStenoperla maclellaniZwick, 1979 were investigated by gut content analysis. Adults were collected throughout New Zealand by light‐trapping at 77 streamside sites most of which were located in native forest.S. prasinawas widely distributed and collected at 43 sites, whereasS. maclellaniwas sampled at 10 sites in the South Island only. Of 200 S. prasinaand 42 S. maclellanidissected, 36% and 69% respectively, contained food. Microscopic examination of a subset of individuals indicated that the gut contents of both species were dominated by sooty mould fungi with lesser contributions made by plant tissue, pollen grains and the spores of tree ferns. These findings suggest that stoneflies had been feeding on the trunks, branches and foliage of trees and perhaps on fronds of tree ferns. As the abdomens of most females were packed with eggs, which mature in late‐instar nymphs it is likely that feeding provides adults with a source of immediately available energy for mating and flight. Encysted larval stages of hairworms (Nematomorpha) and a trematode were also found in both stonefly species. Metacercarial cysts of the trematode are the first records of larval flukes parasitising New Zealand stoneflies. They were found in about 43% of dissected adults of each species with up to 40 cysts present in some individuals. It is possible that the parasite's definitive host is one of New Zealand's native bats (Chiroptera), which are known to eatStenoperlaand inhabit streamside forests at some of the localities where parasitised stoneflies were taken. Overall, our results provide further evidence for the importance of sooty mould fungi as a food source for New Zealand insects and highlight the role ofStenoperlaas a vector of larval parasites from aquatic to terrestrial hosts.

Effects of Inertial Power and Inertial Force on Bat Wings.

The inertial power and inertial force of wings are important factors in evaluating the flight performance of native bats. Based on measurement data of wing size and motions of Eptesicus fuscus, we present a new computational bat wing model with divided fragments of skeletons and membrane. The motions of the model were verified by comparing the joint and tip trajectories with native bats. The influences of flap, sweep, elbow, wrist and digits motions, the effects of different bones and membrane of bat wing, the components on vertical, spanwise and fore-aft directions of the inertial power and force were analyzed. Our results indicate that the flap, sweep, and elbow motions contribute the main inertial power and force; the membrane occupies an important proportion of the inertial power and force; inertial power on flap direction was larger, while variations of inertial forces on different directions were not evident. These methods and results offer insights into flight dynamics in other flying animals and may contribute to the design of future robotic bats.

Bats like vintage: managing exotic eucalypt plantations for bat conservation in a Mediterranean landscape

AbstractThe transformation of native habitats into forest plantations for industrial purposes frequently has negative consequences for biodiversity. We evaluated the impact of eucalypt plantations on native bats in a Mediterranean area, taking Portugal as a case study. We compared the overall bat activity, species richness and Kuhl's bat Pipistrellus kuhlii (the most abundant bat species in the area) activity between eucalypt plantations and native montado habitat, and examined the influence of stand, landscape and survey variables within plantations on the response variables. A set of 11 plantation stands, three landscape and two survey variables were employed as predictor variables using a zero‐inflated Poisson generalized linear mixed model. Hawking and generalist bats of the genus Pipistrellus were the most frequently detected species. Bat activity, species richness and P. kuhlii activity were higher in native montado than in any of the eucalypt stands. Mature eucalypt plantations showed the highest bat activity, while clear‐cut areas showed the lowest. Generally, within eucalypt stands, complex high‐level vegetation structure, from the ground level up to 3 m high, and proximity to water points were associated with higher levels of bat and P. kuhlii activity and species richness. The results suggest that in order to promote bat diversity and activity in exotic eucalypt plantations in the Mediterranean region, it is important to provide a high density of water points, maintain plots of mature plantations and promote understorey clutter.

日本産コウモリのEmbryo-sizeならびにLitter-size (I)

日本産コウモリのEmbryo-sizeならびにLitter-size (I)

Experimental study of European bat lyssavirus type-2 infection in Daubenton's bats (Myotis daubentonii)

European bat lyssavirus type 2 (EBLV-2) can be transmitted from Daubenton's bats to humans and cause rabies. EBLV-2 has been repeatedly isolated from Daubenton's bats in the UK but appears to be present at a low level within the native bat population. This has prompted us to investigate the disease in its natural host under experimental conditions, to assess its virulence, dissemination and likely means of transmission between insectivorous bats. With the exception of direct intracranial inoculation, only one of seven Daubenton's bats inoculated by subdermal inoculation became infected with EBLV-2. Both intramuscular and intranasal inoculation failed to infect the bats. No animal inoculated with EBLV-2 seroconverted during the study period. During infection, virus excretion in saliva (both viral RNA and live virus) was confirmed up to 3 days before the development of rabies. Disease was manifested as a gradual loss of weight prior to the development of paralysis and then death. The highest levels of virus were measured in the brain, with much lower levels of viral genomic RNA detected in the tongue, salivary glands, kidney, lung and heart. These observations are similar to those made in naturally infected Daubenton's bats and this is the first documented report of isolation of EBLV-2 in bat saliva. We conclude that EBLV-2 is most likely transmitted in saliva by a shallow bite.

Susceptibility of sheep to European bat lyssavirus type-1 and -2 infection: A clinical pathogenesis study

European bat lyssaviruses (EBLVs) have been known to cross the species barrier from their native bat host to other terrestrial mammals. In this study, we have confirmed EBLV-1 and EBLV-2 susceptibility in sheep ( Ovis ammon) following intracranial and peripheral (intramuscular) inoculation. Notably, mild clinical disease was observed in those exposed to virus via the intramuscular route. Following the intramuscular challenge, 75% of the animals infected with EBLV-1 and 100% of those that were challenged with EBLV-2 developed clinical signs of rabies and then recovered during the 94-day observation period. Disease pathogenesis also varied substantially between the two viruses. Infection with EBLV-1 resulted in peracute clinical signs, which are suggestive of motor neuron involvement. Antibody induction was observed and substantial inflammatrory infiltrate in the brain. In contrast, more antigen was detected in the EBLV-2-infected sheep brains but less inflammatory infiltrate and no virus neutralising antibody was evident. The latter involved a more protracted disease that was behaviour orientated. A high infectious dose was required to establish EBLV infection under experimental conditions (≥5.0 logs/ml) but the infectious dose in field cases remains unknown. These data confirm that sheep are susceptible to infection with EBLV but that there is variability in pathogenesis including neuroinvasiveness that varies with the route of infection. This study suggests that inter-species animal-to-animal transmission of a bat variant of rabies virus to a terrestrial mammal host may be limited, and may not always result in fatal encephalitis.

Biology and Impacts of Pacific Island Invasive Species. 2. Boiga irregularis, the Brown Tree Snake (Reptilia: Colubridae)1

The Brown Tree Snake, Boiga irregularis (Merrem, 1802), was accidentally transported to the island of Guam shortly after World War II. Over the following two decades it spread throughout the island with little public or professional recognition of its extent or impacts. This secretive nocturnal arboreal snake occurs in all habitats on Guam, from grasslands to forests. Under the right conditions, it is capable of high rates of reproduction and population growth. The Brown Tree Snake caused the extirpation of 13 of Guam's 22 native breeding birds and contributed to the extirpation of several species of native bats and lizards. Guam's 12 forest birds were especially impacted, with 10 species eliminated and the other two severely reduced. In addition, the snake continues to substantially impact domestic poultry, pets, the island's electrical power infrastructure, and human health. To protect other vulnerable Pacific islands, the U.S. government annually spends several million dollars inspecting cargo outbound from Guam to exclude Brown Tree Snakes. Cargo destinations most at risk are in Micronesia, especially the Northern Mariana Islands, but Guam also has direct air transportation links to Hawai‘i that will soon be supplemented with direct ship traffic. Ultimately, all Pacific islands are at risk but especially those obtaining cargo through Guam.

European Bat Lyssaviruses, the Netherlands

To study European bat lyssavirus (EBLV) in bat reservoirs in the Netherlands, native bats have been tested for rabies since 1984. For all collected bats, data including species, age, sex, and date and location found were recorded. A total of 1,219 serotine bats, Eptesicus serotinus, were tested, and 251 (21%) were positive for lyssavirus antigen. Five (4%) of 129 specimens from the pond bat, Myotis dasycneme, were positive. Recently detected EBLV RNA segments encoding the nucleoprotein were sequenced and analyzed phylogenetically (45 specimens). All recent serotine bat specimens clustered with genotype 5 (EBLV1) sequences, and homologies within subgenotypes EBLV1a and EBLV1b were 99.0%-100% and 99.2%-100%, respectively. Our findings indicate that EBLVs of genotype 5 are endemic in the serotine bat in the Netherlands. Since EBLVs can cause fatal infections in humans, all serotine and pond bats involved in contact incidents should be tested to determine whether the victim was exposed to EBLVs.