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Modern phylogeographic methods have confirmed that species with broad ranges often exhibit fine-scale patterns of genetic variation that are not reflected in their morphology. Recent genetic analyses of the straw-colored fruit bat (Eidolon helvum) deviate from this trend in identifying this species as broadly panmictic across its range in Sub-Saharan Africa. However, the limitations of sampling, along with potential for modern anthropogenic impacts to distort observed patterns, suggest that additional work is needed to assess true historical patterns of geographic variation in this species. We used Next Generation Sequencing (NGS) methods to assess patterns of variation found in historical samples of E. helvum and its sister species, E. dupreanum (a Malagasy endemic). Patterns of genomic variation observed among specimens collected between 1909 and 1983 were compared with those from more recently collected tissue samples from across much of the range of the genus. Our genetic analyses confirm that E. helvum and E. dupreanum are distinct species as traditionally recognized. Congruent with results from prior analyses of modern samples, no patterns of spatial genomic structuring were identified in E. helvum across continental Africa in either recent times or earlier in the 20th century. These results suggest that the currently observed pattern of panmixia in E. helvum is not a recent phenomenon; significant gene flow is apparently ongoing in this species across an exceptionally large area. This suggests that potentially zoonotic pathogens previously associated with populations of E. helvum may be similarly distributed or episodically transmitted across broad areas by this species. Our study additionally demonstrates that analyses utilizing ‘archival’ DNA from older specimens in museum collections have the potential to illuminate patterns of both past and contemporary biodiversity, and to help assess the impacts of habitat loss and climate change on species at the genomic level.
Sergei V. Kruskop, Iliya V. Artyushin, Alexandr P. Yuzefovich, Enkhbat Undrakhbayar, Anna S. Speranskya, Alexandra A. Lisenkova, Anna A. Bannikova, Vladimir S. Lebedev
Most of the molecular taxonomic studies on the Eurasian long-eared bats (Plecotus) are based on mitochondrial data only, which might lead to erroneous assessment of the phylogenetic relationships. Here, the genetic divergence among the Mongolian species of Plecotus is examined using sequences of two nuclear introns (THY and ABHD11) and the mitochondrial cytochrome b gene. Both mitochondrial and nuclear data support the existence of three species: Plecotus ognevi, P. kozlovi, and P. turkmenicus. The status of the latter taxon was unclear, as it was previously known from a single record in Mongolia. In our study, P. turkmenicus is found to be widely distributed across the hyperarid deserts south of the Altai Mountains. In several locations, it is sympatric with P. kozlovi, the distribution of which is associated mostly with the semidesert zone, while P. ognevi occurs in the steppe and forest zones of northern Mongolia. The two desert species (P. kozlovi and P. turkmenicus) are quite similar in their morphology and ecological affinities; however, the molecular data clearly show that P. turkmenicus is highly divergent from both P. kozlovi and P. ognevi. In contrast, the mtDNA difference between the arid-dwelling P. kozlovi and the morphologically distant forest-steppe P. ognevi is low. This result demonstrates that more than one lineage of Plecotus independently developed adaptations to the arid habitats of Central Asia and suggests that the morphological similarity between P. kozlovi and P. turkmenicus is a result of convergence. The difference in mtDNA between the Mongolian and West-Central Asian populations of P. turkmenicus indicates that the former may represent a separate taxon of uncertain rank.
Loss of foraging habitat and reductions in insect prey are key factors responsible for declines in bat populations. Identifying important bat foraging habitats and the ecological requirements and conservation status of prey provides evidence for appropriately targeted conservation management strategies. We examined the foraging habits of the barbastelle, Barbastella barbastellus, at the northern edge of its European range using a combination of radio tracking, to determine home range use and habitat selection, and DNA metabarcoding, to identify prey items consumed. Riparian vegetation and broadleaved woodland were the habitat types most strongly selected by foraging bats. Hedgerows within pastoral habitats were also important foraging features within the landscape. We identified 120 different prey items within faecal pellets, the majority of which were moths (97.5%). The large majority (97%) of prey items consumed have larval stages dependent on host plants that are typically found within habitats selected by foraging B. barbastellus. Almost half of all moth prey species identified have undergone considerable population declines in recent decades. We present the most comprehensive list to date of prey consumed by B. barbastellus and provide evidence that conservation management policies should target the protection and enhancement of key B. barbastellus foraging habitats within a 6.5 km sustenance zone around maternity roost sites. Riparian habitat, broadleaved woodland and linear landscape features such as hedgerows should be managed to improve their value to foraging B. barbastellus as well as the developmental stages of their preferred moth prey.
We studied the distribution of an endangered species of bat strongly associated with woods in NW Italy. A species distribution model (SDM) was built on data collected in 2015–2016 using a presence-only technique (maximum entropy) incorporating environmental variables (19 habitat categories, and 4 topography variables). Barbastelle bat presence (132 sites) was associated with woods (beechwoods, oak-hornbeam woods, and wood arboriculture), while there was a negative selection of built or cultivated areas and open space categories. The model was highly successful when predicting the presence/absence of the species in 43 new sites sampled in 2017–2018. SDM was utilized to calculate resistance surfaces and to assess potential suitable connections among the currently utilized areas. The currently protected areas of NW Italy showed a moderate overlap both with high environmental value areas (23.5%) or high connection areas (11.3%). This study highlights a moderate effectiveness of the protected areas network for conservation of barbastelle bat, and suggests preventing land-use change in current woodland areas and increasing connections in the lowland areas of the region. Our results from predicted species occurrence obtained through SDM can be utilized for targeting survey efforts to identify new barbastelle bat sites.
Bats have a major functional role in wetlands; understanding how functional traits of bats depend on environmental characteristics can facilitate management of ecosystems and their services. In this study, we investigated how bat functional diversity has been affected by different anthropogenic impacts in wetlands of the Trans-Andean tropical dry forest of Colombia. Specifically, we analyzed how different functional traits responded to changing environmental conditions and land use and land cover patterns. We sampled six wetlands during the dry periods of the hydrological cycle from 2014 to 2018 and modeled the functional diversity as a function of environmental variables. To understand the association of bat community structure with environmental variables and biotic factors, we combined the RLQ analysis and the fourth-corner approach to relate environmental characteristics and species traits. The percentages of water surface area and pasture land were found to be associated with the general traits of bats when analyzed using the relative abundance of species. In addition, changes in functional diversity appeared to be driven mainly by larger species (e.g., Phyllostomus hastatus, Artibeus lituratus), whose presence was primarily associated with heterogeneous areas. The fourth-corner analysis revealed that the greatest length of skull is the trait that best describes the presence of bats in landscapes of pastures, water bodies, and high abundance of the shrubs Vismia sp. and Cecropia sp. These results suggest that combinations of specific features are important drivers of variation in functional diversity between wetlands. Considering the high vulnerability of Colombian wetlands, our findings provide fundamental information for the development of strategies for monitoring wetland biodiversity. The results can help identify priority conservation sites and improve environmental decision making.
Bats spend half of their lifetime roosting, but their behaviour during this state has not been analysed in most species. The analysis of roosting behaviour is crucial to understand many aspects of bat ecology and social dynamics, but it can be hard to do in natural conditions, especially in cave-dwelling bats. In two species of long-nosed bats (Leptonycteris curasoae and L. yerbabuenae), reproductively active males display a unique smearing behaviour and develop an odoriferous dorsal patch during the reproductive season, presumably involved in female mate choice. As a first step to study the smearing behaviour under controlled conditions, in this study, we analysed the roosting behaviour of a captive group of 18 adult individuals (1:1 sex ratio) of L. curasoae through analysis of day-round (24 hrs) video recordings. We succeeded in producing an ethogram and in estimating the daily time budgets of the group. We also examined the effect of sex and condition of males (with dorsal patch, without dorsal patch) on behaviour. We identified 18 behaviours and classified them into five first-order categories (general maintenance, locomotion, vigilance, social and sexual) and two behavioural states (resting and self-grooming). Behaviours related to muscle and fur maintenance were the most frequent (wing stretching and self-grooming, respectively). Social behaviours (allogrooming and pushing) were relatively infrequent. The latter result suggests loose or cryptic inter-individual liaisons, probably associated with the natural dynamics of colony composition. The main difference between males and females was the expression of hugs (male to female), suggesting that this could be a sexual behaviour (pre-copulatory or pair-bonding). The behaviour of males was independent of the presence of a dorsal patch. We discuss the need for additional research to find the correlates of dorsal patch activity in order to control these variables in future studies aimed to investigate the smearing behaviour in captivity.
Emerging pathogens can cause mass mortalities in susceptible species. High host mortality, in turn, can alter species composition, community structure and function. White-nose syndrome (WNS) is an emerging wildlife disease introduced to North America that has decimated millions of cave-dependent bats. For areas affected by WNS, there have been reports of community compositional changes, but compensatory changes to species composition following WNS has only been suggested, not reported. To determine if compensatory changes to species composition occur following WNS, we used seven years of data from statewide citizen science mobile bat acoustic routes initiated by the Ohio Division of Wildlife in 2011. We hypothesized that migratory bat abundance increased and cave-dependent bat abundance decreased following the emergence of WNS in the study period (2011–2017). Our hypothesis was based on the higher susceptibility of cave-dependent bats than migratory bats to infection and WNS mortality. We used two sets of models to identify abundance trends of each species found in Ohio and species grouped by wintering and roosting behaviors that are putatively important to changes in species composition post-WNS. Following WNS, we found a compensatory change in species in summer months from cave-dependent, cavity-roosting species (Myotis species and Eptesicus fuscus) to migratory, cavity-roosting species (Nycticeius humeralis and Lasionycteris noctivagans). However, for species that roost in foliage in the summer, we did not detect an increase in migratory species (Lasiurus borealis and Lasiurus cinereus) paired with a decrease in cave-dependent species (Perimyotis subflavus). The observed post-WNS trends in bat populations could suggest shifts in bat species composition in other areas where WNS is established.
Occupancy models have not been commonly used in studies focused on bat ecology, although they offer an opportunity to include site covariates along environmental gradients as well as factors that influence detection probability (e.g., lunar illumination). Here we assessed the influence of elevation and forest cover on occupancy and the effect of lunar illumination on detectability of bat species in the Northern Andes of Peru. We captured 1,052 bats, belonging to three families and 26 species, over two survey periods (2008–2010 and 2014–2015) at 14 sites. The most detected species were the frugivorous Artibeus glaucus, Carollia brevicauda, C. perspicillata, Platyrrhinus ismaeli, P. nigellus, Sturnira erythromos, and S. oporaphilum. Detection probability (p) of both Artibeus planirostris, C. brevicauda and C. perspicillata were significantly related to the survey period, while S. erythromos and S. oporaphilum detectability was associated with lunar illumination. Elevation was marginally positively associated with S. erythromos occupancy, with a moderate relative explanatory power based on AICc weight. We did not find support for an effect of forest cover on bat occupancy. The estimation of both bat occupancy (Ψ) and detectability (p) provides the basis for the design of monitoring programs with a spatiotemporal approach and constitutes a critical component in the context of land-use change and changing climate. For bat species in montane habitats, we suggest that S. erythromos is a useful species for use in monitoring programs, based on both occupancy, and detection probability, as well as its adaptability to montane areas.
Pups of bats emit isolation calls and the precursor of echolocation calls (echolocation precursors) during postnatal growth. Isolation calls are used by neonates to solicit maternal care. In some species, isolation calls contain individual signatures that allow the mother bat to distinguish its own offspring from others. Little is known, however, about whether echolocation precursors also contain individual signatures. This study examined the postnatal growth and ontogeny of vocalizations in free-ranging Kerivoula furva, a social bat that uses the furled leaves of banana plants as day roosts. We tested the hypothesis that echolocation precursors of K. furva pups contain individual signatures. We found pups of K. furva emitted both isolation calls and echolocation precursors on the day of birth, indicating the two types of call develop independently. The call parameters of the echolocation precursors changed as pups aged, with the frequency increasing and pulse duration decreasing. The echolocation precursors resemble adult echolocation calls when pups reach approximately 25–30 days old. The results also showed the parameters of echolocation precursors differ significantly among pups that roosted together. We suggest echolocation precursors might function as communication signals for mother-offspring recognition.
Acoustic monitoring provides an effective and non-invasive means to survey many species such as bats, birds and frogs. However, the acoustic monitoring poses challenges in determining the species identity due to lack of reference recordings or due to similar call structures across species. Here we recorded bats from 30 different locations at varying altitudes (0–1,200 m) and latitudes (7–12°N) using a full spectrum Pettersson M500-384 ultrasound detector. We used 2,070 pulses from 329 individual sequences of 20 bat species to standardise the echobank (catalogue of call characteristics). Discriminant function analyses (DFA) was carried out separately for the bats producing constant frequency (CF) and frequency modulated (FM) calls using frequency of maximum energy and end frequency, and shows an accuracy of 97.48% and 96.09% for CF and FM bats respectively. We also collated published reference calls for bat species in this region to develop a regional echobank for 42 species of echolocating bats from the Western Ghats. For six species, we report their echolocation calls for the first time. The echobank provides a useful tool for further conservation and monitoring studies in the wider region.
Bats are a highly diverse order with substantial economic and ecological value. Similarly, forests in South Africa form a valuable biome supporting unique biotic diversity, yet forest bat communities have not previously been surveyed. We sampled 17 forests, of seven forest types and three forest groups, in the Eastern Cape and southern KwaZulu-Natal provinces, located within the Maputaland-Pondoland-Albany global biodiversity hotspot. We utilized capture and acoustic survey methods to compile the first bat species inventory for these forests. Species identification was performed with a combined approach of morphology, echolocation, and DNA barcodes. With this we contributed novel DNA barcodes to the Barcode of Life Data System. A total of 25 species was recorded, with range extensions southward into the Eastern Cape for six species, indicating the region to be more diverse than previously thought. Updated modelled distribution maps for these species are presented. We compiled the first reference call library of hand released bats for South African forest habitats, and the southeast region of the country. We compared species richness, diversity, and dissimilarity of the forest types and found that Scarp forests host the highest species richness and diversity. Patterns of species assemblage similarities between forest groups are attributed to forest biogeographical history and historical dispersal routes of forest fauna. A comprehensive survey, such as this, may assist in the compilation and implementation of forest conservation management plans and future monitoring programs.
Winter counts in bat hibernacula are a standard method to monitor their populations. However, it is unclear to what degree counting bats in hibernacula triggers energy consuming arousals in hibernating bats. This study quantifies the reaction of three hibernating bat species (Pipistrellus sp., Myotis nattereri, and Plecotus auritus) to a monitoring survey in a hibernaculum complex consisting of eight modified bunkers in northern Germany. Skin temperatures of hibernating bats were measured with a thermal camera at the beginning and end of each visit to quantify the proportion of individuals that elevated their body temperatures during the visit. Moreover, bat activity was recorded using light barriers placed at the entrances of the hibernacula. According to the thermal camera measurements, eight of 1,849 individuals in Pipistrellus spp. (0.4%) and one of 47 individuals of M. nattereri (2.1%) elevated their body temperature during the monitoring. The median number of light barrier passes similarly increased slightly from seven to nine on monitoring days compared to control days. Notably, general linear models suggest that the effect of monitoring was less severe with rising ambient temperatures. Our results suggest that bat monitoring in hibernacula is unlikely to threaten winter survival in hibernating bats if carried out responsibly, and the number and duration of human visits are kept to a minimum.
Although cliffs may play an important role in bat ecology (offering natural roosting sites and thermally favourable foraging habitat), there are surprisingly few systematic investigations of bat activity in cliff habitats compared to other habitats. We carried out systematic recordings of bat calls at inland cliff habitats (comprising natural cliffs and quarries) and compared them to three other habitat types (water bodies, settlements and forests) in order to better understand the importance of cliff habitats for bats. A total of 38,440 call sequences were recorded during this study. Overall bat activity at cliff habitats was comparable to activity at water bodies and settlements but was much higher compared to forests. Median activity in forests was only 6% of that in other habitat types. In total, we recorded a minimum of 19 bat species (16 determined to the species level and three representing indistinguishable species pairs). At cliff habitats, 18 species were recorded, representing at least 75% of the 24 bat species with recent records from Carinthia, Austria, including many threatened species. Two species exhibited a significant preference for cliffs over other habitat types: Eptesicus serotinus and Hypsugo savii, the latter of which is known to be a cliff habitat specialist. Bat assemblages in cliff habitats and settlements tended to be more similar compared to other habitat types, a finding that may contribute to our understanding of the urban ecology of bats. The results of our study emphasise the importance of inland cliff habitats for bats and thus, the preservation of abandoned quarries is a significant conservation measure for bats. Moreover, studies focusing on possible negative impacts of rock climbing on bat activity and roosting behaviour of bats are needed.
Leandra R. Palheta, Gustavo L. Urbieta, Leandro S. Brasil, Karina Dias-Silva, Jennifer B. Da Silva, Gustavo Graciolli, Ludmilla M. S. Aguiar, Thiago B. Vieira
Bats and bat flies are intimately associated and are relevant models to study the effects of anthropogenic impacts when bats are highly distributed in urban environments. The lack of knowledge on bat's responses to the anthropogenic effects as related to their bat flies leads to ineffective conservation strategies. Thus, our goal is to describe the association between bats and bat flies in urban and non-urban environments and measuring how much urbanization can alter the parasite-host associations. We collected bats and bat flies in 11 sites (six urban areas and five non-urban areas) distributed among five municipalities of the state of Pará. To identify a possible pattern on communities, we conducted a Composition Principal Component Analysis and performed a permutational multivariate analysis of variance using distance matrices — PERMANOVA. We captured 513 bats and examined 867 bat flies. Our findings show that bat and bat fly communities of rural environments in the Amazon are more diverse than those from urban environments. Urbanization seems to play an essential role as an environmental filter of bats and bat fly species that are exclusively rural.
The increase in human population has resulted in environmental alterations and habitat fragmentation, such as those caused by road construction. Since the late 1990s, there has been an increase in studies evaluating the effects of roads on vertebrate populations; however, few studies have considered bats in road ecology studies. In this review on road ecology studies focusing on bats, we evaluated the impacts of roads on bat mortality, commuting, and foraging. We also evaluated the use of road structures as roosts and provide suggestions for future research and mitigation methods based on available results. Road impacts on bat activity and roadkill are strongly influenced by landscape features, and areas with short trees have more impact on roadkill. Also, in open areas, bats prefer to forage near roads whereas in woodland areas activity increases with distance from the road. Most studies evaluating the effects of roads on bats have been conducted in Europe, therefore it is essential that these studies are conducted in other areas, especially in developing countries. To ensure the conservation of bat species, it is imperative that studies consider all impacts that roads have on bat populations and that mitigation measures are applied, especially when road construction meets bat commuting or foraging paths.
Carlos H. S. Silva, Maria S. M. Amarante, Eugenia Cordero-Schmidt, Juan C. Vargas-Mena, Marília A. S. Barros, Sirlene S. R. Sartori, Danielle B. Morais
In view of the great diversity of dietary habits among bats, and the need for morphological adaptations in their digestive system, this study characterized and compared the morphology of the small (SI) and large intestines (LI) of the bats Artibeus planirostris (Phyllostomidae: Stenodermatinae) and Diphylla ecaudata (Phyllostomidae: Desmodontinae), and interpret their morphologies in the context of dietary differences. We hypothesized that diet could influence the morphological characteristics in these two species by means of a more complex intestinal morphology in A. planirostris than in D. ecaudata. The intestines were histologically processed, stained, and analyzed. Despite body mass differences, total intestinal length were almost two folds higher in A. planirostris than in D. ecaudata, and the intestinal coefficient, which quantifies the investment in intestines in relation to the body mass, wasn't statistically different. Macroscopically, no distinction was observed between the SI and LI, and few differences allowed to distinguish histologically the regions of the SI in both species. We found a typical organization of Peyer's patches only in D. ecaudata. Enteroendocrine cells were more frequently observed at caudal parts of the small intestine in both species. In A. planirostris, the SI diameter, the thickness of its wall, and the thickness and percentage occupied by the mucosal layer, as well as the wall thickness of its LI, were greater than those in D. ecaudata. Circular folds were observed only in the LI of A. planirostris. We speculate that these differences represent strategies to increase the contact surface available to optimize nutrient uptake in A. planirostris; while the hematophagous feeding habit of D. ecaudata, predominantly proteinaceous and semifluid, has a gut wall characterized with less morphological complexity and specializations; which confirms our hypothesis. Based on the similarities and differences founded, it can be concluded for both species that the reduction in the anatomical structures, associated with the microscopic findings, allows to optimize the absorption of nutrients and water in these bats when compared to other mammals; a similar pattern to that found in other chiropterans.
Bats are the second most diverse and widely distributed group of mammals, and may be directly or indirectly involved in some zoonotic diseases. Their baseline hematological knowledge and health condition in natural populations are important parameters, but when bats and humans cohabitate common spaces such as houses, buildings, and recreational parks, these variables become essential. Blood samples of bats representing 16 species from families Phyllostomidae (nine species; n = 104 individuals), Noctilionidae (two species; n = 24), and Molossidae (five species; n = 9) were obtained from 137 individuals captured in human-related spaces mostly in Mérida state, Venezuela. Hematocrit (Hct), total white blood cell counts (WBC), and differential white blood cell counts (DWBC) were quantified, and profiles compared in groups with large samples sizes and unambiguous reproductive conditions. Also, a general examination of blood smears was performed to assess the viability of in situ hemopathogen identification. Hct (x̄ ± SEM) of bats was 51.0 ± 1.9% for Artibeus lituratus (n = 53) and 51.0 ± 3.8% for A. jamaicensis (n = 18), the two most common bat species captured. WBC were higher in Phyllostomidae than in the other two families, and most species exhibited a DWBC formula dominated by lymphocytes. Lactating and pregnant females of A. lituratus showed higher values of neutrophiles than males and non-reproductive females. Overall, blood cell morphology and hematological profiles were consistent with those of other species of bats and/or mammals. Hemopathogens were observed in 19 individuals from three species. In this study, we report Anaplasma-compliant observations in blood samples of bats, but this first report requires molecular validation and further research to expand the knowledge on hemopathogens of bats. Our research is an important contribution to the hematological characterization of common species of Neotropical bats, and the first in providing hematological data for six species from three families of bats.
The diversity of bat species and some of their distinct biological and ecological characteristics contribute to their wide distribution, being generally abundant and common in a variety of habitats, factors that can influence their association with different emerging and reemerging viruses. Studies have shown that bats have characteristics which contribute to the evolution of a unique set of antiviral immune responses that control the replication of viruses, such as their gregarious social organization and ability to fly. In this paper we review the incidence of viruses in Neotropical bats, and the role of species as hosts or vectors of these diseases. A total of 110 species belonging to seven families were found to have been detected carrying virus in the region. Although Chiroptera is the second most diverse order of mammals, the diversity of bat-hosted viruses has only recently come into focus, as the result of improved wildlife surveillance. Diverse viruses have been detected in bats, however, in the majority of the cases, there is no evidence that the virus is transmitted from bats to other animals or causes disease in humans.
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