Miniopterus Research Articles

First Evidence of Antibodies Against Lloviu Virus in Schreiber's Bent-Winged Insectivorous Bats Demonstrate a Wide Circulation of the Virus in Spain.

Although Lloviu virus (LLOV) was discovered in the carcasses of insectivorous Schreiber’s Bent-winged bats in the caves of Northern Spain in 2002, its infectivity and pathogenicity remain unclear. We examined the seroprevalence of LLOV in potentially exposed Schreiber’s Bent-winged bats (n = 60), common serotine bats (n = 10) as controls, and humans (n = 22) using an immunoblot assay. We found antibodies against LLOV GP2 in all of Schreiber’s Bent-winged bats serum pools, but not in any of the common serotine bats and human pools tested. To confirm this seroreactivity, 52 serums were individually tested using Domain Programmable Arrays (DPA), a phage display based-system serology technique for profiling filovirus epitopes. A serological signature against different LLOV proteins was obtained in 19/52 samples tested (36.5%). The immunodominant response was in the majority specific to LLOV-unique epitopes, confirming that the serological response detected was to LLOV. To our knowledge, this is the first serological evidence of LLOV exposure in live captured Schreiber’s Bent-winged bats, dissociating LLOV circulation as the cause of the previously reported die-offs.

Phylogeography of Miniopterus fuliginosus (Chiroptera) with special reference to Jeju Island, South Korea

Abstract To better understand the genetic relatedness of the eastern bent-wing bat Miniopterus fuliginosus across East Asia, mitochondrial D-loop sequences were analyzed from 39 M. fuliginosus individuals living on Jeju Island, South Korea. Seven different haplotypes were identified. Neighbor-joining analysis was performed and divergence time was calculated in combination with available online data on D-loop and ND2 sequences of M. fuliginosus in East Asia, respectively. Results suggest that M. fuliginosus populations living on Jeju Island and in Japan originated from China in the past 20,000 years.

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.

Eastern Bent-winged Bat observed at Sakura Cho,Hadano City

Eastern Bent-winged Bat observed at Sakura Cho,Hadano City

Mitochondrial DNA marker (D-loop) reveals high genetic diversity but low population structure in the pale bent-wing bat (Miniopterus pallidus) in Iran

This study investigates the population genetic structure of Miniopterus pallidus using the D-loop region of mitochondrial DNA (331 bp) from 13 localities in Iran. We found a high number of haplotypes (N = 43) and high nucleotide diversity (π = 0.02). The average K2P genetic distance was high within (2.59%) and between (2.54%) the Iranian populations of M. pallidus and analysis of molecular variance revealed that most genetic variability was related to differences within populations. The positive and significant association between pairwise genetic and environmental distances (r = 0.443, p = .01) after accounting for the effect of geographical distances suggests that substantial influence of the climatic factors among different sites have shaped the genetic variation in this species. Neutrality tests showed historical demographic events when applying Fu’s Fs, but Tajima’s statistic was nonsignificant, indicating a deviation from the theoretical model of expansion. The hypothesis of sudden-expansion was not rejected by analyses of mismatch distribution as the Raggedness and SSD were insignificant (p(r)= .39 and p(SSD) = .38). Similarly, BSP results approximately revealed a major historical expansion around 81,000 years ago and a recent population decline around 13,000 years ago. Phylogenetic trees illustrated that all Iranian M. pallidus populations, as well as those from eastern Turkey and Azerbaijan, form a monophyletic clade, whereas the samples from western Turkey, Georgia and Greece belong to M. schreibersii clade. The haplotype network was consistent with these findings for M. pallidus populations in Iran and showed a high level of reticulation.

Polychromophilus melanipherus and haemoplasma infections not associated with clinical signs in southern bent-winged bats (Miniopterus orianae bassanii) and eastern bent-winged bats (Miniopterus orianae oceanensis).

While bats are often viewed as carriers of infectious disease agents, little research has been conducted on the effects these pathogens may have on the bat populations themselves. The southern bent-winged bat (Miniopterus orianae bassanii) is a critically endangered subspecies endemic to south-eastern Australia. Population numbers of this bat have declined over the past 50 years, but the reasons for this are unclear. As part of a larger study to determine if disease could be a contributing factor to this decline, southern bent-winged bats from several locations in Victoria and South Australia were captured and examined for the presence of the blood parasite, Polychromophilus melanipherus, and haemoplasmas (Mycoplasma sp.). Results were compared with those obtained from populations of the more common, partially sympatric, eastern bent-winged bat (Miniopterus orianae oceanensis) from three different locations in Victoria. Both organisms were found in both subspecies (prevalence of P. melanipherus 60% by PCR for southern bent-winged bats compared with 46% for eastern bent-winged bats; prevalence of haemoplasmas 10% for southern bent-winged bats compared with 8% for eastern bent-winged bats), with no association between the probability of infection, body weight, abnormal blood parameters or any other indicators of ill health. However, Victorian southern bent-winged bats had heavier burdens of P. melanipherus than both the South Australian southern bent-winged bats and eastern bent-winged bats. Further investigations are required to determine if these differences are impacting population health.

Encephalomyocarditis virus is potentially derived from eastern bent-wing bats living in East Asian countries

Bats are reservoir hosts of many zoonotic viruses and identification of viruses that they carry is important. This study aimed to use high throughput screening to identify the viruses in fecal guano of Taiwanese insectivorous bats caves in order to obtain more information on bat-derived pathogenic viruses in East Asia. Guano samples were collected from two caves in Taiwan, pooled, and then subjected to Multiplex PCR-based next generation sequencing for viral identification. Subsequently, encephalomyocarditis virus (EMCV) sequence was detected and confirmed by reverse transcription PCR. EMCV is considered as rodent virus and thus, animal species identification through cytochrome oxidase I (COI) barcoding was further done to identify the viral source. Finally, determination of distribution and verification of the presence of EMCV in guano obtained from Japanese and South Korean caves was also done. We concluded that the guano collected was not contaminated with the excrement of rodents which were reported and presumed to live in Taiwan. Also, EMCV genome fragments were found in guanos of Japanese and South Korean caves. It is possible that the eastern bent-wing bat (Miniopterus fuliginosus) is one of the natural hosts of EMCV in East Asia.

Ectoparasites are unlikely to be a primary cause of population declines of bent-winged bats in south-eastern Australia.

While bats carry a diverse range of ectoparasites, little research has been conducted on the effects these organisms may have on bat populations. The southern bent-winged bat (Miniopterus orianae bassanii) is a critically endangered subspecies endemic to south-eastern Australia, whose numbers have declined over the past 50 years for unknown reasons. As part of a larger study to investigate the potential role of disease in these declines, southern bent-winged bats from four locations were captured and examined for the presence of bat flies, mites, ticks and the nematode Riouxgolvania beveridgei (previously associated with skin nodules in bent-winged bats). Results were compared with those obtained from the more common eastern bent-winged bat (Miniopterus orianae oceanensis), sampling animals from three different locations. All four types of parasite were found on both subspecies. There was no correlation between the presence of ectoparasites, body weight or any signs of disease. However, prevalence of tick and R. beveridgei infections were greater in Victorian southern bent-winged bats than South Australian southern bent-winged bats and eastern bent-winged bats, possibly indicative of some type of chronic stress impacting the immune system of this subspecies.

Lowland rainforest bat communities of Ulu Temburong National Park with two new records for Brunei Darussalam

Tropical rainforest ecosystems have high levels of both animal and plant biodiversity with many aspects of their ecology understudied. In particular, extensive research is still required to gather accurate estimates of distribution and abundance of forest-interior bat species in Borneo. Accurate abundance data and further knowledge of individual species’ ecology is vital for implementing effective conservation. Bats were captured using a harp trap, set up along established trails and around buildings, at Kuala Belalong Field Studies Centre, Ulu Temburong National Park, Brunei Darussalam between 14th-19th January 2018. Ulu Temburong National Park is comprised of pristine primary mixed dipterocarp lowland rainforest that has not been exposed to logging or fragmentation. A total of nine bat species were recorded, with two new records for Brunei, Miniopterus australis (Lesser bent-winged bat, N = 1) and Myotis horsfieldii (Horsfield’s myotis, N = 5). Furthermore, a coincidental sighting of a colony of Megaderma spasma roosting on the mangrove island Selirong, in Temburong District is reported here. The bat species captured and encountered in this small-scale study expand our understanding of bat communities in Temburong as well as indicate that current records for the area are far from complete. This affirms the need for further work in building up accurate abundance and diversity estimates, both for Ulu Temburong National Park and Brunei Darussalam.

Virus survey in populations of two subspecies of bent-winged bats (Miniopterus orianae bassanii and oceanensis) in south-eastern Australia reveals a high prevalence of diverse herpesviruses.

While bats are often viewed as carriers of infectious disease agents, little research has been conducted on the effects these potential pathogens may have on the bat populations themselves. The southern bent-winged bat (Miniopterus orianae bassanii) is a critically endangered subspecies endemic to south-eastern Australia. Population numbers of this bat have been declining for the past 50 years, but the reasons for this are unclear. As part of a larger study to determine if disease could be a contributing factor to this decline, 351 southern bent-winged bats from four locations were captured, and oral swabs were collected and tested for the presence of potentially pathogenic viruses. Results were compared with those obtained from 116 eastern bent-winged bats (Miniopterus orianae oceanensis) from three different locations. The eastern bent-winged bat is a related but more common and widespread subspecies whose geographical range overlaps partly with southern bent-winged bats. Herpesviruses were detected in bent-winged bats from all seven locations. At least six novel herpesviruses (five betaherpesviruses and one gammaherpesvirus) were identified. The prevalence of herpesvirus infection was higher in eastern bent-winged bats (44%, 51/116), compared to southern bent-winged bats (27%, 95/351), although this varied across the locations and sampling periods. Adenoviruses and a range of different RNA viruses (lyssaviruses, filoviruses, coronaviruses and henipaviruses) were also tested for but not detected. The detected herpesviruses did not appear to be associated with obvious ill health, and may thus not be playing a role in the population decline of the southern bent-winged bat. The detection of multiple novel herpesviruses at a high prevalence of infection is consistent with our understanding of bats as hosts to a rich diversity of viruses.

Illustrated redescription of the male of Ixodes simplex Neumann, 1906

Ixodes simplex is a tick species of bats, mainly reported from Schreibers’ Bent-winged bat, Miniopterus schreibersii, all over its host’s range. While being a common parasite of cave-dwelling bat species, the initial description of males is poor (based on a sole damaged specimen), lacking distinctive features. This study describes the male of I. simplex also providing measurements for a number of characters, using a series 10 of specimens. Males of I. simplex show the following characteristics distinct from males of I. ariadnae and I. vespertilionis: idiosoma is shorter (2.6 mm vs. 3.4–4.7 mm); the palps of I. simplex males are laterally curved (bent) (while straight in I. ariadnae and gradually curving in I. vespertilionis), the genital opening is anterior in position between coxae II (whereas posterior to second intercoxal space in I. vespertilionis); coxae II are to some extent rectangular (vs. rounded in I. ariadnae); coxae IV have a prominent tuft of long hairs (missing in the other two species). Most importantly, the legs of I. simplex males are considerably shorter than in males of the other two species (2.7–3.3 mm vs. 7–10 mm). The description is completed with high-quality pictures highlighting all the mentioned features.

Geographical variation in the echolocation calls of bent-winged bats, Miniopterus fuliginosus

Evolutionary biologists had a long-standing interest in the evolutionary forces underlying geographical variation in the acoustic signals of animals. However, the evolutionary forces driving acoustic variation are still unclear. In this study, we quantified the geographical variation in the peak frequencies of echolocation calls in eight Miniopterus fuliginosus bat colonies, and assessed the forces that drive acoustic divergence. Our results demonstrated that seven of the colonies had very similar peak frequencies, while only one colony was significantly higher than the others. This similarity in echolocation call frequency among the seven colonies was likely due to frequent dispersal and migration, leading to male-mediated infiltration of nuclear genes. This infiltration enhances gene flow and weakens ecological selection, and also increases interactions in the presence of conspecifics. Significant correlations were not observed between acoustic distances and morphological distances, climatic differences, geographic distances or mtDNA genetic distances. However, variation in acoustic distances was significantly positive correlated with nDNA genetic distance, even after controlling for geographic distance. Interestingly, the relationship between call divergence and genetic distance was no longer significant after excluding the colony with the highest call frequency, which may be due to the minimal genetic distance among the other seven colonies. The highest frequencies of echolocation calls observed in the one colony may be shaped by selection pressure due to loud background noise in the area. Taken together, these results suggest that geographic divergence of echolocation calls may not be subject to genetic drift, but rather, that the strong selective pressure induced by background noise may lead to acoustic and genetic differentiation between JXT and the other colonies.

Agriculture shapes the trophic niche of a bat preying on multiple pest arthropods across Europe: Evidence from DNA metabarcoding.

The interaction between agricultural production and wildlife can shape, and even condition, the functioning of both systems. In this study, we i) explored the degree to which a widespread European bat, namely the common bent-wing bat Miniopterus schreibersii, consumes crop-damaging insects at a continental scale, and ii) tested whether its dietary niche is shaped by the extension and type of agricultural fields. We employed a dual-primer DNA metabarcoding approach to characterize arthropod 16S and COI DNA sequences within bat faecal pellets collected across 16 Southern European localities, to first characterize the bat species' dietary niche, second measure the incidence of agricultural pests across their ranges and third assess whether geographical dietary variation responds to climatic, landscape diversity, agriculture type and vegetation productivity factors. We detected 12 arthropod orders, among which lepidopterans were predominant. We identified >200 species, 44 of which are known to cause agricultural damage. Pest species were detected at all but one sampling site and in 94% of the analysed samples. Furthermore, the dietary diversity of M. schreibersii exhibited a negative linear relation with the area of intensive agricultural fields, thus suggesting crops restrict the dietary niche of bats to prey taxa associated with agricultural production within their foraging range. Overall, our results imply that M. schreibersii might be a valuable asset for biological pest suppression in a variety of agricultural productions and highlight the dynamic interplay between wildlife and agricultural systems.

First record of Trypanosoma dionisii of the T. cruzi clade from the Eastern bent-winged bat (Miniopterus fuliginosus) in the Far East

Chiropteran mammals worldwide harbour trypanosomes (Euglenozoa: Kinetoplastea: Trypanosomatida) of the subgenus 'Schizotrypanum' in the classical sense. Latterly, these trypanosomes have been referred to as members of the 'Trypanosoma cruzi clade' as their phylogenetic relationships, structure and life cycle conform to T. cruzi, parasitising various terrestrial mammals as well as humans in Latin America. Little is known, however, about the trypanosome species in Asian bats. During a survey on Borrelia spp. in the Eastern bent-winged bat (Miniopterus fuliginosus) living in a cave in Wakayama Prefecture, Japan, incidental proliferation of trypanosomes was detected in two of 94 haemocultures. Squat or slender trypanosomes that proliferated in the cultures were 7.5-20.5μm in length between both body ends and 1.0-3.8μm in width with/without free flagella up to 14.5μm (n= 29). The nucleotide sequences of the small subunit ribosomal RNA gene (SSU rDNA; 2176bp), large subunit ribosomal RNA gene (1365bp) and glycosomal glyceraldehyde-3-phosphate dehydrogenase gene (gGAPDH; 843bp) of the present isolates were characterized to clarify their molecular phylogenetic position in T. cruzi-like trypanosomes. The newly obtained SSU rDNA and gGAPDH nucleotide sequences showed the highest identities with Brazilian and European isolates of Trypanosoma dionisii of the T. cruzi clade, ranging between 99.4 and 99.7% or between 95.6 and 99.3% identities, respectively. Although multiple T. dionisii isolates from the North and South American continents showed the closest molecular genetic relatedness to the present Far East isolates, only short SSU rDNA segments of the former isolates were deposited. Therefore, a definitive conclusion cannot be made until full nucleotide sequencing of at least the American isolates' SSU rDNA is available. This is the first confirmation of a Far East distribution of T. dionisii, demonstrating a wide geographical distribution of the species in the Eurasian and American continents with a limited nucleotide variation.

Wind turbines impact bat activity, leading to high losses of habitat use in a biodiversity hotspot

Previous studies have mainly focused on bat mortality through collision by wind turbines, and very few studies have assessed the indirect impacts on bat activity and on foraging habitat availability. Also, there is a global lack of knowledge on the vulnerability of tropical bat fauna due to wind energy production, even though it is well known that windpower can affect bat communities and biodiversity hotspots are widespread in the tropics. We present one of the first studies to quantify the indirect impact of wind farms on insectivorous bats in tropical hotspots of biodiversity. Bat activity was compared between wind farm sites and control sites, via ultrasound recordings at stationary points. The activity of bent winged bats (Miniopterus sp.) and wattled bats (Chalinolobus sp.) were both significantly lower at wind turbine sites. The result of the study demonstrates a large effect on bat habitat use at wind turbines sites compared to control sites. Bat activity was 20 times higher at control sites compared to wind turbine sites, which suggests that habitat loss is an important impact to consider in wind farm planning We strongly recommend that the loss of the foraging habitat loss is considered in mitigation hierarchy (avoiding, reducing, offsetting) when compensating for negative impacts of wind farms.

Complete Genome Sequence of Lleida Bat Lyssavirus.

ABSTRACTAll lyssaviruses (family Rhabdoviridae) cause the disease rabies, an acute progressive encephalitis for which, once symptoms occur, there is no effective cure. Using next-generation sequencing, the full-genome sequence for a novel lyssavirus, Lleida bat lyssavirus (LLEBV), from the original brain of a common bent-winged bat has been confirmed.

The genetic diversity of D-loop sequences in eastern bent-winged bats (Miniopterus fuliginosus) living in Wakayama Prefecture, Japan.

The eastern bent-winged bat (Miniopterus fuliginosus) is an insectivorous bat that lives in the caves, throughout Japan [11]. The bats aggregate in cave in populations of tens to thousands of individuals. We examined the mitochondrial D-loop sequences of bats in Wakayama, Japan, and divided them into 35 haplotypes. The sequences of 3 haplotypes in Wakayama were the same as those of 10 Miniopterus fuliginosus individuals living in China. Given the substitution rate of the D-loop region, we speculated that the bats had moved between Japan and China within the last 16,000 years. We could not determine how the bats crossed the sea; however, it is possible that the bats undergo dynamic movement widely throughout East Asia.

РАСПРОСТРАНЕНИЕ И ЭКОЛОГИЯ ОБЫКНОВЕННОГО ДЛИННОКРЫЛА (MINIOPTERUS SCHREIBERSI) В РЕСПУБЛИКЕ АРЦАХ

The paper presents the data obtained as a result of long-term studies of the common bentwing bat (Miniopterus schreibersi (Khul, 1819)) in the Republic of Artsakh. Data on ecology, biology and activity of these animals are given, special attention was paid to the population inhabiting the Azokh cave. In addition, the sex ratio in different populations was studied, and the average life span of these bats was also determined.

Assessment of mercury exposure and maternal-foetal transfer in Miniopterus schreibersii (Chiroptera: Miniopteridae) from southeastern Iberian Peninsula.

Mercury (Hg) is a highly toxic and widely distributed metal that is bioaccumulated in insectivorous mammals and may cause adverse effects on the reproductive system. Bats are considered excellent Hg bioindicators due to their wide distribution, life span, trophic position, metabolic rate and food intake. However, few studies have analysed Hg residues in bats, and to the best of our knowledge, no studies have been made in the Iberian Peninsula. The main aim of this study was to undertake the first ever assessment of Hg exposure in Schreiber's bent-winged bats inhabiting a natural cave in the southeast of Spain. The findings suggest that Schreiber's bent-winged bats in the sampling area are chronically exposed to low levels of Hg. The Hg concentrations found in different tissues (fur, kidney, liver, muscle and brain) were below the threshold levels associated with toxic effects in mammals. Non-gestating females showed Hg concentrations in the brain and muscle that doubled those found in gestating females. This could be due to Hg mobilization from the mother to the foetus in gestating females, although other factors could contribute to explain this result such as variations in hunting areas and the insect-prey consumed and/or different energetic needs and average food consumption during the breeding season. Hg levels were 1.7 times higher, although not significant, in foetus' brains than in the maternal brains, and Hg concentration in foetus' brain was significantly correlated with levels in the corresponding mothers' kidney. These results suggest that there could be an active mother-to-foetus transfer of Hg in bats, which would be of special relevance in a scenario of higher Hg exposure than that found in this study. However, further research is needed to support this view due to the limited number of samples analysed. Given the scarce ecotoxicological data available for bats and their protected status, we encourage further opportunistic studies using carcasses found in the field, the validation of non-destructive samples such as fur and guano for Hg monitoring, and new modelling approaches that will increase the data needed for proper ecological risk assessment in bat populations.

Bats adjust their pulse emission rates with swarm size in the field.

Flying in swarms, e.g., when exiting a cave, could pose a problem to bats that use an active biosonar system because the animals could risk jamming each other's biosonar signals. Studies from current literature have found different results with regard to whether bats reduce or increase emission rate in the presence of jamming ultrasound. In the present work, the number of Eastern bent-wing bats (Miniopterus fuliginosus) that were flying inside a cave during emergence was estimated along with the number of signal pulses recorded. Over the range of average bat numbers present in the recording (0 to 14 bats), the average number of detected pulses per bat increased with the average number of bats. The result was interpreted as an indication that the Eastern bent-wing bats increased their emission rate and/or pulse amplitude with swarm size on average. This finding could be explained by the hypothesis that the bats might not suffer from substantial jamming probabilities under the observed density regimes, so jamming might not have been a limiting factor for their emissions. When jamming did occur, the bats could avoid it through changing the pulse amplitude and other pulse properties such as duration or frequency, which has been suggested by other studies. More importantly, the increased biosonar activities may have addressed a collision-avoidance challenge that was posed by the increased swarm size.