Insectivorous Bats Research Articles

Detection of coronaviruses in insectivorous bats of Fore-Caucasus, 2021

Coronaviruses (CoVs) pose a huge threat to public health as emerging viruses. Bat-borne CoVs are especially unpredictable in their evolution due to some unique features of bat physiology boosting the rate of mutations in CoVs, which is already high by itself compared to other viruses. Among bats, a meta-analysis of overall CoVs epizootiology identified a nucleic acid observed prevalence of 9.8% (95% CI 8.7–10.9%). The main objectives of our study were to conduct a qPCR screening of CoVs’ prevalence in the insectivorous bat population of Fore-Caucasus and perform their characterization based on the metagenomic NGS of samples with detected CoV RNA. According to the qPCR screening, CoV RNA was detected in 5 samples, resulting in a 3.33% (95% CI 1.1–7.6%) prevalence of CoVs in bats from these studied locations. BetaCoVs reads were identified in raw metagenomic NGS data, however, detailed characterization was not possible due to relatively low RNA concentration in samples. Our results correspond to other studies, although a lower prevalence in qPCR studies was observed compared to other regions and countries. Further studies should require deeper metagenomic NGS investigation, as a supplementary method, which will allow detailed CoV characterization.

Identification of coronaviruses in bats and rodents in northern and central Argentina.

Due to the present pandemic situation and the many animal species that are epidemiologically involved, there has been a surge of renewed interest in investigating the coronavirus (CoV) population circulating in wildlife, especially bats and rodents, which are potential reservoirs of new human pathogens. In Argentina, information about the viruses present in these mammals is very limited. To investigate the presence of coronaviruses in this country, we obtained 457 samples from hematophagous, insectivorous, and frugivorous bats and rodents from two regions of Argentina. We report here the detection of alphacoronavirus sequences in three groups of bats as well as in rodents. Phylogenetic analysis showed the closest relationships to alphacoronaviruses from Brazil.

The fecal bacterial microbiome of the Kuhl’s pipistrelle bat (Pipistrellus kuhlii) reflects landscape anthropogenic pressure

BackgroundAnthropogenic disturbance has the potential to negatively affect wildlife health by altering food availability and diet composition, increasing the exposure to agrochemicals, and intensifying the contact with humans, domestic animals, and their pathogens. However, the impact of these factors on the fecal microbiome composition of wildlife hosts and its link to host health modulation remains barely explored. Here we investigated the composition of the fecal bacterial microbiome of the insectivorous bat Kuhl’s pipistrelle (Pipistrellus kuhlii) dwelling in four environmental contexts with different levels of anthropogenic pressure. We analyzed their microbiome composition, structure and diversity through full-length 16S rRNA metabarcoding using the nanopore long-read sequencer MinION™. We hypothesized that the bacterial community structure of fecal samples would vary across the different scenarios, showing a decreased diversity and richness in samples from disturbed ecosystems.ResultsThe fecal microbiomes of 31 bats from 4 scenarios were sequenced. A total of 4,829,302 reads were obtained with a taxonomic assignment percentage of 99.9% at genus level. Most abundant genera across all scenarios were Enterococcus, Escherichia/Shigella, Bacillus and Enterobacter. Alpha diversity varied significantly between the four scenarios (p < 0.05), showing the lowest Shannon index in bats from urban and intensive agriculture landscapes, while the highest alpha diversity value was found in near pristine landscapes. Beta diversity obtained by Bray–Curtis distance showed weak statistical differentiation of bacterial taxonomic profiles among scenarios. Furthermore, core community analysis showed that 1,293 genera were shared among localities. Differential abundance analyses showed that the highest differentially abundant taxa were found in near pristine landscapes, with the exception of the family Alcaligenaceae, which was also overrepresented in urban and intensive agriculture landscapes.ConclusionsThis study suggests that near pristine and undisturbed landscapes could promote a more resilient gut microbiome in wild populations of P. kuhlii. These results highlight the potential of the fecal microbiome as a non-invasive bioindicator to assess insectivorous bats’ health and as a key element of landscape conservation strategies.

Vanilla Bats: Insectivorous Bat Diversity in the Vanilla Agroecosystems of Northeastern Madagascar

Due to global agricultural expansion and intensification, many animal species must now survive within a landscape dominated by agroecosystems. For bats, agroecosystems can provide a valuable foraging-habitat, and many species of bats thrive within such habitats whilst also providing a range of ecosystem services for farmers. Despite this, bat usage of many agroecosystem types remains unstudied. Here, we investigated the diversity of insectivorous bats in the vanilla agroecosystems of northeastern Madagascar, the world's principal vanilla-growing region. To assess bat diversity, we used a passive acoustic survey technique, and we identified and classified bat species diversity using PCA and DFA analysis of echolocation call acoustic parameters. In total, we were able to detect the presence of at least 13 different bat species within Madagascar's vanilla agroecosystems, seven of which we were able to confidently identify to species level. However, due to our conservative classification approach, the true diversity of bats in vanilla agroecosystems is likely to be higher. The results of this study indicate that Madagascar's vanilla agroecosystems represent suitable foraging habitat for numerous bat species, particularly forest-specialists, which is a highly encouraging finding for the conservation of Madagascar's bats. Expansion of vanilla agroecosystems is therefore likely to provide valuable habitat extensions for Madagascar's forest bats in the future, provided this expansion does not come at the expense of existing largely-undisturbed natural habitats.

Temporal partitioning of Bullacris unicolor (Orthoptera: Pneumoridae) calling activity to avoid predation

ABSTRACT Ecological interactions, including competition, predation, and environmental conditions, may significantly impact acoustic signalling behaviour. Here we characterise nocturnal signalling patterns in the bladder grasshopper Bullacris unicolor and relate this to biotic and abiotic factors, thus providing insights into ecological drivers of acoustic signalling behaviour. Passive acoustic recorders monitored nocturnal calling activity of the focal species, competitors, and predatory bats across the distribution of B. unicolor. Results indicate that B. unicolor calls preferentially at certain times of the night, but that peak activity period varies across the geographic range. There was a strong relationship between B. unicolor activity and bat activity. Bullacris unicolor populations further north showed an overall avoidance of bat echolocation call period, whereas further south an overlapping of call periods between B. unicolor and bat echolocation was observed. Bats at northern sites showed a distinct activity period early in the night and B. unicolor may thus reduce predation risk by shifting signalling activity to later in the night. In contrast, bats were active throughout the night at southern sites and B. unicolor did not delay calling activity in this region of its distribution, although the species did shift signalling slightly to reduce peak overlap with co-existing pneumorid species.

Non-destructive methods to assess pesticide exposure in free-living bats

Bat populations are dwindling worldwide due to anthropogenic activities like agriculture, however the role that pesticide exposure plays on these declines is unclear. To address these research gaps, we first need to develop reliable methods to detect and monitor exposure to environmental pollutants and its effects on free-living bats. The use of biomarkers is a sensitive and informative tool to study sublethal effects in wildlife, however it requires laboratory validation and integrative approaches to be applicable to free-living species. In this study, we propose a set of non-destructive biomarkers to evaluate pesticide exposure in free-ranging bats and validated their suitability with dose-exposure experiments in captivity. We selected three biomarkers that have been widely used in vertebrate ecotoxicology and that combined represent sensitive, specific, and ecologically relevant responses to pollutants: DNA damage, AChE activity, and leukocyte profiles. We used two insectivorous bat species as model species Eptesicus fuscus (laboratory) and Pteronotus mexicanus (field). We found that micronuclei frequency (genotoxicity) and AChE activity (exposure and neurotoxicity) were robust indicators of toxicant exposure. The validity of this set of endpoints was supported by their consistent performance in laboratory and field experiments as well as by the significant correlation among them. Leukocyte profile (systemic stress) results were not consistent between laboratory and field studies, suggesting further evaluation of its suitability is needed. Integrative approaches, like the one we used here, maximize the insights about toxicant effects by combining the information of single biomarkers into more meaningful inferences, which can be applied to environmental risk assessments in wildlife. Furthermore, the use of non-destructive, cost-effective biomarkers is imperative when assessing toxicant exposure and effects in vulnerable wildlife and it should be a priority in the field of wildlife toxicology.

Thermal Stability of Contractile Proteins in Bat Wing Muscles Explains Differences in Temperature Dependence of Whole-Muscle Shortening Velocity.

AbstractMuscle contractile properties are dependent on temperature: cooler temperatures generally slow contractile rates. Contraction and relaxation are driven by underlying biochemical systems, which are inherently sensitive to temperature. Carollia perspicillata, a small Neotropical bat, experiences large temperature differentials among body regions, resulting in a steep gradient in temperature along the wing. Although the bats maintain high core body temperatures during flight, the wing muscles may operate at more than 10°C below body temperature. Partially compensating for these colder operating temperatures, distal wing muscles have lower temperature sensitivities in their contractile properties, including shortening velocity, relative to the proximal pectoralis. Shortening velocity is correlated with the activity of myosin ATPase, an enzyme that drives the cross-bridge cycle. We hypothesized that the thermal properties of myofibrillar ATPase from the pectoralis and forearm muscles of the bat wing would correlate with the temperature sensitivity of those muscles. Using myofibrillar ATPases from the proximal and distal muscles, we measured enzyme activity across a range of temperatures and enzyme thermal stability after heat incubation across a range of time points. We found that forearm muscle myofibrillar ATPase was significantly less thermally stable than pectoralis myofibrillar ATPase but that there was no significant difference in the acute temperature dependence of enzyme activity between the two muscles.

Coronaviruses Are Abundant and Genetically Diverse in West and Central African Bats, including Viruses Closely Related to Human Coronaviruses.

Bats are at the origin of human coronaviruses, either directly or via an intermediate host. We tested swabs from 4597 bats (897 from the Democratic Republic of Congo (DRC), 2191 from Cameroon and 1509 from Guinea) with a broadly reactive PCR in the RdRp region. Coronaviruses were detected in 903 (19.6%) bats and in all species, with more than 25 individuals tested. The highest prevalence was observed in Eidolon helvum (239/733; 39.9%) and Rhinolophus sp. (306/899; 34.1%), followed by Hipposideros sp. (61/291; 20.9%). Frugivorous bats were predominantly infected with beta coronaviruses from the Nobecovirus subgenus (93.8%), in which at least 6 species/genus-specific subclades were observed. In contrast, insectivorous bats were infected with beta-coronaviruses from different subgenera (Nobecovirus (8.5%), Hibecovirus (32.8%), Merbecovirus (0.5%) and Sarbecovirus (57.6%)) and with a high diversity of alpha-coronaviruses. Overall, our study shows a high prevalence and genetic diversity of coronaviruses in bats and illustrates that Rhinolophus bats in Africa are infected at high levels with the Sarbecovirus subgenus, to which SARS-CoV-2 belongs. It is important to characterize in more detail the different coronavirus lineages from bats for their potential to infect human cells, their evolution and to study frequency and modes of contact between humans and bats in Africa.

Predator-prey traits and foraging habitat shape the diet of a common insectivorous bat

Individual and species traits may determine the functional relationships between predators and their prey, with clear consequences for the ecosystem services potentially associated with predation. Bats are well-known potential deliverers of ecosystem services in agroecosystems through predation of pest arthropods that may affect crop production. Here we test the role of individual and prey traits in shaping the dietary habits of the Savi's pipistrelle (Hypsugo savii), a common bat species that frequently occurs in agroecosystems across the Mediterranean area, assessing diet composition and trait-based biases through molecular tools and multivariate testing techniques. DNA metabarcoding identified 173 distinct prey taxa in bats sampled in the Vesuvius National Park (Southern Italy). The diet was strongly dominated by pest insects associated with agricultural areas, which covered 57% of the overall prey diversity, some representing major pests of high economic relevance. The multivariate analyses detected strong relationships between diet composition, sampling date, and individual bat body conditions. Larger bats consumed larger prey items, and prey consumed later in the season (August) were smaller than those eaten in early summer (July) and were typical of less natural habitats. Hypsugo savii is potentially an important pest suppressor in the agroecosystems of the Mediterranean region and the functional relationships between the traits of individual bats and their prey set the basis for a quantitative assessment of the associated ecosystem service. We also remark on the value of bat diet studies in aiding the surveillance of arthropod species relevant to agriculture, human health, and biodiversity conservation.

Effect of environmental gradients on community structuring of aerial insectivorous bats in a continuous forest in Central Amazon

Effect of environmental gradients on community structuring of aerial insectivorous bats in a continuous forest in Central Amazon

Visual detection threshold in the echolocating Daubenton's bat (Myotis daubentonii).

All bats possess eyes that are of adaptive value. Echolocating bats have retinae dominated by rod photoreceptors and use dim light vision for navigation, and in rare cases for hunting. However, the visual detection threshold of insectivorous echolocating bats remains unknown. Here, we determined this threshold for the vespertilionid bat Myotis daubentonii. We show that for a green luminous target, M. daubentonii has a visual luminance threshold of 3.2(±0.9)×10-4cdm-2, an intensity corresponding to the luminance of an open cloudless terrestrial habitat on a starlit night. Our results show that echolocating bats have good visual sensitivity, allowing them to see during their active periods. Together with previous results showing that M. daubentonii has poor visual acuity (∼0.6 cycles deg-1), this suggests that echolocating bats do not use vision to hunt but rather to orient themselves.

Vibroacoustic Response of the Tympanic Membrane to Hyoid-Borne Sound Generated during Echolocation in Bats.

The hyoid apparatus in laryngeally echolocating bats is unique as it forms a mechanical connection between the larynx and auditory bullae, which has been hypothesized to transfer the outgoing echolocation call to the middle ear during call emission. Previous finite element modeling (FEM) found that hyoid-borne sound can reach the bulla at an amplitude likely heard by echolocating bats; however, that study did not model how or if the signal could reach the inner ear (or cochlea). One route that sound could take is via stimulation of the eardrum-similarly to that of air-conducted sound. We used micro computed tomography (μCT) data to build models of the hyoid apparatus and middle ear from six species of bats with variable morphology. Using FEM, we ran harmonic response analyses to measure the vibroacoustic response of the tympanic membrane due to hyoid-borne sound generated during echolocation and found that hyoid-borne sound in all six species stimulated the eardrum within a range likely heard by bats. Although there was variation in the efficiency between models, there are no obvious morphological patterns to account for it. This suggests that hyoid morphology in laryngeal echolocators is likely driven by other associated functions.

Molecular evidence of Borrelia spp. in bats from Córdoba Department, northwest Colombia

BackgroundThe genus Borrelia is composed of two well-defined monophyletic groups, the Borrelia burgdorferi sensu lato complex (Bb) and the relapsing fever (RF) group borreliae. Recently, a third group, associated with reptiles and echidnas, has been described. In general, RF group borreliae use rodents as reservoir hosts; although neotropical bats may also be involved as important hosts, with scarce knowledge regarding this association. The objective of this study was to detect the presence of Borrelia spp. DNA in bats from the department of Córdoba in northwest Colombia.MethodsDuring September 2020 and June 2021, 205 bats were captured in six municipalities of Córdoba department, Colombia. Specimens were identified using taxonomic keys and DNA was extracted from spleen samples. A Borrelia-specific real-time PCR was performed for the 16S rRNA gene. Fragments of the 16S rRNA and flaB genes were amplified in the positive samples by conventional PCR. The detected amplicons were sequenced by the Sanger method. Phylogenetic reconstruction was performed in IQ-TREE with maximum likelihood based on the substitution model TPM3+F+I+G4 with bootstrap values deduced from 1000 replicates.ResultsOverall, 10.2% (21/205) of the samples were found positive by qPCR; of these, 81% (17/21) and 66.6% (14/21) amplified 16S rRNA and flaB genes, respectively. qPCR-positive samples were then subjected to conventional nested and semi-nested PCR to amplify 16S rRNA and flaB gene fragments. Nine positive samples for both genes were sequenced, and seven and six sequences were of good quality for the 16S rRNA and flaB genes, respectively. The DNA of Borrelia spp. was detected in the insectivorous and fruit bats Artibeus lituratus, Carollia perspicillata, Glossophaga soricina, Phyllostomus discolor, and Uroderma sp. The 16S rRNA gene sequences showed 97.66–98.47% identity with “Borrelia sp. clone Omi3,” “Borrelia sp. RT1S,” and Borrelia sp. 2374; the closest identities for the flaB gene were 94.02–98.04% with “Borrelia sp. Macaregua.” For the 16S rRNA gene, the phylogenetic analysis showed a grouping with “Candidatus Borrelia ivorensis” and “Ca. Borrelia africana,” and for the flaB gene showed a grouping with Borrelia sp. Macaregua and Borrelia sp. Potiretama. The pathogenic role of the Borrelia detected in this study is unknown.ConclusionsWe describe the first molecular evidence of Borrelia spp. in the department of Córdoba, Colombia, highlighting that several bat species harbor Borrelia spirochetes.Graphical

Rhipicephalus microplus larvae: first report in bats, Molossus rufus.

Cattle are the main hosts of Rhipicephalus microplus; however, this ixodid can also parasitize other animal species. We collected a specimen of R. microplus larvae from one bat Molossus rufus (Mammalia, Chiroptera) from the Cachoeirinha municipality (29° 56' 52'' S and 51° 5' 43'' W), Rio Grande do Sul, Brazil. The specimen was taxonomically identified using identification keys(Vargas2006). This study reports the first occurrence of this species parasitizing insectivorous bats in Brazil.

Basidiobolomycosis: a case of a rare fungal infection misdiagnosed as adenocarcinoma of the colon

Background: Basidiobolomycosis is a rare infection caused by the fungus Basidiobolus ranarum. Since 1887, B. ranarum has been identified as an unusual fungus. It is a saprophytic fungus found in soil, decaying fruits and vegetables, and the digestive tracts of amphibians, fish, reptiles, and insectivorous bats. Since its discovery in 1964, this unusual and rare fungal infection has only been reported 71 times in the literature, and few cases were reported in Saudi Arabia. Case Presentation: A 62-year-old female Burmese with a 2-month history of nausea, vomiting, diarrhea, and chronic abdominal pain, accompanied by weight loss, loss of appetite, and lower limb myopathy was pre sented. This myopathy was so severe that it rendered her bedridden, thereby diminishing her quality of life. No hemoptysis or bleeding per rectum was seen. Past surgical and medical history were unremarkable. No med ications or allergies were reported. Regarding her social history, she was married and a housewife with low socioeconomic status, and a significant language barrier. The patient was successfully diagnosed and properly treated. Conclusion: Basidiobolomycosis is an emerging fungal pathogen. It usually causes subcutaneous infection, transmitted via traumatic inoculation. Gastrointestinal basidiobolomycosis is rare; it is associated with mass or inflammatory lesions in the gastrointestinal tract.

Bats in the Maldives: a review of historical data and first record of a vagrant Long-winged Tomb Bat (Emballonuridae: Taphozous longimanus)

The Maldives is a country made up entirely of coral atolls with very limited terrestrial habitat diversity and only one known resident bat species: the Maldivian Flying Fox, Pteropus medius ariel. Here we report the first confirmed record of any insectivorous bat from the Maldives: a single bat that flew on board a boat off Raa Atoll in the north of Maldives on 13 February 2019. Wind trajectory analysis suggests that it had flown from Kerala, south India. From photos and morphometric estimates, we could identify it as a Long-winged Tomb Bat Taphozous longimanus. Reports of Flying Foxes from the Maldives (P. medius ariel and P. hypomelanus maris) are also reviewed. The former is widespread and common, while the latter is known only from a single disputed and now apparently missing specimen.

Seasonal analysis of the diet and trophic niche breadth of Molossus rufus É. Geoffroy, 1805 (Mammalia: Chiroptera) in a tropical urban environment.

This study aimed to analyze the diet and trophic niche breadth of an insectivorous bat very common in an urban environment in southern Brazil. To analyze the feeding habit of Molossus rufus, it was necessary to collect fecal samples in urban colonies in the city of Maringá, State of Paraná. Samplings occurred from November 2018 to September 2019, including rainy and dry seasons. The fragments found in the samples were identified up to the level of order or family whenever possible. Percentage of volume and frequency of occurrence, Feeding Index (IAi%), PERMANOVA, and trophic niche breadth were used. Thus, a total of 140 samples were obtained, 92 for the rainy season and 48 for the dry season. In terms of percentage of volume, the diet consisted mainly of Hymenoptera (46.9%) in the rainy season and Coleoptera (39.2%) in the dry season. The results for standardized trophic niche breadth were Ba = 0.36 for the rainy season and Ba = 0.37 in the dry season, indicating a low food diversity. In conclusion, there was a food preference on the part of M. rufus according to the season evaluated, with Hymenoptera and Coleoptera being the most relevant dietary items.

Caudal auricular muscle variations and the evolution of echolocation behavior in pteropodid bats.

Among bats, rhinolophoids and yangochiropterans, but not pteropodids, exhibit laryngeal echolocation. Although Rousettus has been regarded as the only pteropodid capable of echolocation using tongue clicks, recent evidence suggests that other species of pteropodids are also capable of echolocation using wing clicks. Studies on laryngeal echolocators suggest that delicate ear movements are essential for the echolocation behavior of bats and that the cervicoauricularis muscles play a critical role in such ear movements. In this study, we observed the gross anatomy of cervicoauricularis muscles in three species of pteropodids (Cynopterus sphinx, Eonycteris spelaea, and Rousettus leschenaultii) to examine whether ear muscle anatomy varies among pteropodids with different echolocation types and between pteropodids and laryngeal echolocating bats. We found that M. cervicoauricularis profundus originates from the nuchal crest in tongue-click echolocators (R. leschenaultii) and from the midline in wing-click echolocators (C. sphinx and E. spelaea). In general, tongue-click echolocation using high click rates is considered to be more sophisticated in terms of sonar performance than wing-click echolocation. M. cervicoauricularis profundus originating from the nuchal crest (CPNC) is not common in non-bat laurasiatherian mammals, but can be found in laryngeal echolocating bats. As it pulls the ear pinna caudally in the horizontal plane and increases the access to sound, CPNC found in R. leschenaultii and laryngeal echolocating bats may be a key characteristic of the sophisticated active echolocation behavior of bats.

Adaptive transformations of the organism of the Small Bat (Pipistrellus pygmaeus) under conditions of combined negative anthropogenic factors

Chiropteran mammals have unique body anatomy features that are adapta- tions for flight. However, the histophysiological, physiological, and biochemical parameters of bats have not been studied enough, including under the influence of anthropogenic fac- tors. The article presents the results of a morphological study of the internal organs and hematological and biochemical studies of the blood of bats (using the example of the small bat), living in the Bryansk region, under conditions of technogenic and anthropogenic load. During the work, somatometric measurements of the body and the measurement of the linear parameters of the internal organs were determined. Hematological and biochemical studies of the blood of the small bat were carried out on an automatic biochemical analyzer according to generally accepted methods. Morphological and anatomical adaptation of the small bat, which ensures compliance with the structure of the body and its mode of action, is manifested in the dynamics of somatometric indicators of the body, in the plasticity of macro- and micrometric indicators of the kidneys and liver. Physiological adaptation that maintains the functional state is manifested in quantitative and qualitative reactions from the cellular elements of the blood, demonstrating higher values. It has been established that the number of erythrocytes in the blood of male and female bats is directly dependent on sex, physiological state and age.

Distribution of the bat Family Mormoopidae in Honduras

Honduras is the second country in central America along with Panamá with the greatest bat diversity, and the insectivorous bats are the most diverse in the Chiroptera order. The family Mormoopidae has the largest number of records in Honduras and these bats are important as pest control in crops where they are present. To understand the importance of the Mormoopidae family in Honduras, we need to know where it is distributed. A species distribution model is a tool that provides information on the distribution of the species, based on presences records and climate variables. We collected information from free access databases like GBIF, reports, and paper publication to obtain presence data in Honduras. To run the models, we used Maxent in dismo package. Our results show a similar distribution for all species of Mormoopidae family, the principal causes that limited the distribution of the species are ecosystem type and altitude; some species tolerated evergreen forest and others prefer dry forest, in terms of elevation, in some species is limited from lowland to 1500 m.a.s.l., like Mormoops megalophylla, Pteronotus psilotis, and Pteronotus gymnonotus, and others can inhabit above 2800 m.a.s.l., like Pteronotus fulvus, and Pteronotus mesoamericanus. We need to obtain more records of species like M. megalophylla, P. psilotis, and P. gymnonotus. More surveys in the eastern part of Honduras are necessary where there are many information gaps, this would help us to have more robust models and a better understanding of the distribution of these species.