Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: implications for conservation

Fourteen species of bats are reported for the first time from Guyana (Saccopteryx gymnura, Micronycteris brachyotis, M. homezi, Lichonycteris obscura, Anoura latidens, Vampyressa pusilla, Vampyrodes caraccioli, Eptesicus chiriquinus, Cynomops paranus, Molossops neglectus, Molossus sp., Molossus coibensis, Molossus sinaloae, and Promops centralis) bringing the known bat diversity for the country to 121 species. Information including measurements, reproductive data, distribution, and taxonomy are provided for these species. Seven of these new records were collected in the Iwokrama International Rain Forest Programme site in central Guyana. Eighty-six bat species are now documented from Iwokrama Forest which is the highest species diversity for bats reported from any protected area in the world. There are, however, few tropical sites that have relatively complete inventories. A summary for bat species diversity in southern Venezuela, Guyana, Suriname, and French Guiana indicates that at least 146 species of bats are known from the Guianan subregion. Intense inventory surveys, especially in the often neglected subcanopy, suggest that species richness is probably underestimated in most Neotropical areas. Likewise, species-level diversity in the Guianan subregion is higher than previously suggested. Surveying and monitoring biodiversity are critical to developing a National Protected Areas System in Guyana.     

Distribution of cave-dwelling bats and conservation status of underground habitats in the Istanbul area

Populations of cave-dwelling bat species were investigated in the transitory region between the Eastern Thrace and the Western Pontus. Data were collected during 30 surveys in 13 underground sites, 10 of which had not been surveyed previously by bat researchers, between March 1999 and March 2000. Approximately 20 000 bats representing eight species were recorded. Grouping the sites according to their ecological resemblance, by means of cluster and correspondence analyses, yielded different results for the summer and winter data. In summer, there was a partial separation of the sites by their location in biogeographic regions. In winter, no regional grouping was observed. It was concluded that in the transitory region, species distribution does not differ considerably between the Eastern Thracian and Western Pontic ecosystems. In addition, a conservation scoring system is proposed for those sites investigated, their status is evaluated, and the most important local roosts are identified.     

Ecological zoogeography of the bats of Paraguay

Aim To relate the composition of bat assemblages in Paraguay to environmental factors (vegetation) and to test the hypothesis that the observed patterns of distribution of Paraguayan mammals is ultimately due to soils and geological features. Location Paraguay. Methods Museum specimens were used to create a data base of 3762 individuals of forty-eight species collected in twenty-six 50 × 50 km sites distributed throughout the country. Proportion of each of sixteen vegetation types per site was estimated from vegetation maps. Vegetation and bat data were related using canonical correspondence analysis (CCA) and Mantel tests. The same analyses were performed with the bat data grouped in terms of trophic strategies. Results A significant relationship was found between composition of vegetation and composition of bat assemblages. CCA ordination arranged plant associations and bat assemblages into three distinct groups: Dry Chaco, Floodable Lands and Eastern Paraguay, which correspond to the major characteristics of the Paraguayan vegetation, geology and soils. Frugivorous bats were restricted to Eastern Paraguay and Floodable Lands, whereas most insectivore and omnivore species occur across the entire country. However, the maximum abundance of insectivorous and omnivorous species within each genus indicates that there is at least a partial segregation of species to one of the three regions, and in those cases where the maximum abundance of congeneric species coincide, those species differ considerably in size. Main conclusions The Paraguayan bat fauna is a composite of species from various South American biomes, with no endemic species. However, species are not randomly distributed across the country despite the lack of geographical barriers and the high dispersal capabilities of bats. Instead, species presence at any given site is strongly associated with vegetation patterns that are ultimately the result of the geological history of the area. This correlation can be explained partially in terms of habitat suitability and resource availability. Additionally, results suggest that interspecific interactions are also an important component in determining the composition of a given bat assemblage.     

Characterization of dinucleotide microsatellite loci in big brown bats (Eptesicus fuscus), and their use in other North American vespertilionid bats

We describe the development of six microsatellite loci for big brown bats, Eptesicus fuscus. Microsatellite markers were isolated from a small insert genomic library, and tested on a population of 44 animals from the Pend d’Oreille Valley, in southeastern British Columbia, Canada. These six loci were highly variable, with 12–23 alleles per locus, and observed and expected heterozygosities of greater than 79.5%. The six primer sets, and three others that were not variable in E. fuscus, were tested on 11 other species in the families Vespertilionidae and Antrozoidae. All the tested loci amplified highly variable products in at least several other species.     

Stage of pregnancy dictates heterothermy in temperate forest-dwelling bats

Bats face high energetic requirements, as powered flight is costly and they have a disadvantageous surface-to-volume-ratio. To deal with those requirements energy saving mechanisms, such as heterothermy (torpor), have evolved. Torpor during pregnancy, however, reduces rates of foetal development and consequently prolongs pregnancy. Therefore, heterothermy has a great effect on reproduction, as an unhindered parturition can only be assured by high body temperatures. Regardless of these adverse affects of torpor the energetic requirements of bats during reproduction urge for energy savings and bats are known to enter torpor during pregnancy. The species in the current study differ in their torpor patterns and thus their heterothermic strategy. However, we hypothesized, that species-specific heterothermic behaviour should be revoked at the end of pregnancy. We analyzed skin temperatures of Myotis bechsteinii, Myotis nattereri and Plecotus auritus during pregnancy and found no differences in torpor depth between species during the last phase of pregnancy. Furthermore, we could show that individuals entered torpor frequently during pregnancy and only minimized torpor during the last stage of pregnancy. This suggests that close to the end of pregnancy, heterothermy is restricted but not species-specific and the required energy is allocated otherwise.     

Analysis of the distribution of insectivorous bats in Israel

Data on localities from which insectivorous bats were collected or sighted in Israel were compiled into a Geographical Information System (GIS) in order to analyse patterns of species distribution. By intersecting precipitation and temperature data with spatially-referenced data on species observations stored in the GIS we determined the 'climatic envelope' of each species and constructed predictive maps which show the potential distribution of each species. Using cluster analysis, the bats were classified into three main biogeographic groups according to their distribution, namely desert, Mediterranean, and widespread in Israel. The potential distribution maps of all the species indicate that there are areas which have suitable bat habitats but from which bats have never been collected or observed. In the Mediterranean region of Israel, this is attributed to a large reduction in population size due to fumigation of caves, cave visitation and secondary poisoning.     

The impact and implications of climate change for bats

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Reproduction elevates the corticosterone stress response in common fruit bats

Changes in reproductive state or the environment may affect the sensitivity of the hypothalamic-pituitary-andrenal (HPA) axis. However, little is known about the dynamics of the resulting corticosteroid stress response, in particular in tropical mammals. In this study, we address the modulation of corticosterone release in response to different reproductive conditions and seasonality in 326 free-living common fruit-eating bats (Artibeus jamaicensis) on Barro Colorado Island in Panama during dry and wet seasons. We present strong evidence that stress sensitivity is primarily modulated by reproductive condition. In reproductively active females, corticosterone increases were more rapid and reached higher levels, but also decreased significantly faster than in inactive females. The corticosterone response was weaker in reproducing males than in females and delayed compared to non-reproductive males. Testes volume in reproductively active males was negatively correlated with corticosterone concentrations. Our findings suggest differentiated dynamics in the corticosterone stress response between sexes, potentially reflecting conflicting ecological demands. In females, a strong acute corticosterone response may represent high stress- and risk-sensitivity that facilitates escape and thus helps to protect reproduction. In males, suppression during reproductive activity could reflect lowered stress sensitivity to avoid chronically elevated corticosterone levels in times of frequent aggressive and therefore costly inter-male encounters.     

Extremely variable di‐ and tetranucleotide microsatellite loci in Brazilian free‐tailed bats (Tadarida brasiliensis)

We present three dinucleotide and six tetranucleotide microsatellite loci that were developed for the Brazilian free‐tailed bat, Tadarida brasiliensis (Chiroptera, Molossidae). Ninety‐one individuals from two populations were scored at each locus, revealing extremely high levels of polymorphism (15–55 alleles per locus). These loci provide genetic markers for studying gene flow, migration and mating behaviour.     

Foraging shifts and visual preadaptation in ecologically diverse bats

Changes in behaviour may initiate shifts to new adaptive zones, with physical adaptations for novel environments evolving later. While new mutations are commonly considered engines of adaptive change, sensory evolution enabling access to new resources might also arise from standing genetic diversity, and even gene loss. We examine the relative contribution of molecular adaptations, measured by positive and relaxed selection, acting on eye‐expressed genes associated with shifts to new adaptive zones in ecologically diverse bats from the superfamily Noctilionoidea. Collectively, noctilionoids display remarkable ecological breadth, from highly divergent echolocation to flight strategies linked to specialized insectivory, the parallel evolution of diverse plant‐based diets (e.g., nectar, pollen and fruit) from ancestral insectivory, and—unusually for echolocating bats—often have large, well‐developed eyes. We report contrasting levels of positive selection in genes associated with the development, maintenance and scope of visual function, tracing back to the origins of noctilionoids and Phyllostomidae (the bat family with most dietary diversity), instead of during shifts to novel diets. Generalized plant visiting was not associated with exceptional molecular adaptation, and exploration of these novel niches took place in an ancestral phyllostomid genetic background. In contrast, evidence for positive selection in vision genes was found at subsequent shifts to either nectarivory or frugivory. Thus, neotropical noctilionoids that use visual cues for identifying food and roosts, as well as for orientation, were effectively preadapted, with subsequent molecular adaptations in nectar‐feeding lineages and the subfamily Stenodermatinae of fig‐eating bats fine‐tuning pre‐existing visual adaptations for specialized purposes.     

Roads and bats: a meta‐analysis and review of the evidence on vehicle collisions and barrier effects

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Seasonal variation in age,sex, and reproductive status of Mexican free-tailed bats

In North America, Mexican free-tailed bats (Tadarida brasiliensis mexicana) consume vast numbers of insects contributing to the economic well-being of society. Mexican free-tailed bats have declined due to historic guano mining, roost destruction, and bioaccumulation of organochlorine pesticides. Long-distance migrations and dense congregations at roosts exacerbate these declines. Wind energy development further threatens bat communities worldwide and presents emerging challenges to bat conservation. Effective mitigation of bat mortality at wind energy facilities requires baseline data on the biology of affected populations. We collected data on age, sex, and reproductive condition of Mexican free-tailed bats at a cave roost in eastern Nevada located 6 km from a 152-MW industrial wind energy facility. Over 5 years, we captured 46,353 Mexican free-tailed bats. Although just over half of the caught individuals were nonreproductive adult males (53.6%), 826 pregnant, 892 lactating, 10,101 post-lactating, and 4327 nonreproductive adult females were captured. Juveniles comprised 11.5% of captures. Female reproductive phenology was delayed relative to conspecific roosts at lower latitudes, likely due to cooler temperatures. Roost use by reproductive females and juvenile bats demonstrates this site is a maternity roost, with significant ecological and conservation value. To our knowledge, no other industrial scale wind energy facilities exist in such proximity to a heavily used bat roost in North America. Given the susceptibility of Mexican free-tailed bats to wind turbine mortality and the proximity of this roost to a wind energy facility, these data provide a foundation from which differential impacts on demographic groups can be assessed.     

A practical sampling design for acoustic surveys of bats

Acoustic surveys are widely used for describing bat occurrence and activity patterns and are increasingly important for addressing concerns for habitat management, wind energy, and disease on bat populations. Designing these surveys presents unique challenges, particularly when a probabilistic sample is required for drawing inference to unsampled areas. Sampling frame errors and other logistical constraints often require survey sites to be dropped from the sample and new sites added. Maintaining spatial balance and representativeness of the sample when these changes are made can be problematic. Spatially balanced sampling designs recently developed to support aquatic surveys along rivers provide solutions to a number of practical challenges faced by bat researchers and allow for sample site additions and deletions, support unequal-probability selection of sites, and provide an approximately unbiased local neighborhood-weighted variance estimator that is efficient for spatially structured populations such as is typical for bats. We implemented a spatially balanced design to survey canyon bat (Parastrellus hesperus) activity along a stream network. The spatially balanced design accommodated typical logistical challenges and yielded a 25% smaller estimated standard error for the mean activity level than the usual simple random sampling estimator. Spatially balanced designs have broad application to bat research and monitoring programs and will improve studies relying on model-based inference (e.g., occupancy models) by providing flexibility and protection against violations of the independence assumption, even if design-based estimators are not used. Our approach is scalable and can be used for pre- and post-construction surveys along wind turbine arrays and for regional monitoring programs. © 2011 The Wildlife Society.     

Parasitization of bats by bat flies (Streblidae) in fragmented habitats

Parasites represent a large fraction of the world's biodiversity. They control host population sizes and contribute to ecosystem functioning. However, surveys on species diversity rarely include parasitic species. Bats often present traits favoring parasite diversity, such as large home ranges, long life spans, and large colonies. The most conspicuous bat parasites are the highly host-specific, blood-sucking bat flies (Diptera: Streblidae, Nycteribiidae). Recent studies have found a direct effect of habitat alteration on the abundance of bat species. We expected, therefore, that changes in the host community in response to anthropogenic habitat modification will also result in changes in the associated parasite community. We captured bats in three different habitats in Central Panama between 2013 and 2015. We recorded information on prevalence and intensity of bat fly parasitization of the seven most commonly captured bat species. Prevalence and intensity were both significantly influenced by roost type, abundance, and host sex and age. We found that habitat variables and matrix type significantly influenced the prevalence and intensity of parasitization, while the direction of the responses was host species- and parasite species-specific. In general, roosting conditions and behavior of host bats appear to be fundamental in explaining changes in prevalence and intensity of parasitization between different habitat types, as bat flies are bound to the roost during their reproductive cycle. Habitat alterations affect next to the host community composition also the availability of possible roost structures as well as microclimatic conditions, which all three reflect in parasitization.     

Tent-roosting may have driven the evolution of yellow skin coloration in Stenodermatinae bats

The recent discovery of the first mammal that deposits significant amounts of carotenoid pigments in the skin (the Honduran white bat Ectophylla alba) has highlighted the presence of conspicuous yellow coloration in the bare skin of some bats. This is patent in the subfamily Stenodermatinae, where many species build tents with plant leaves for communal roosting at daytime. On the basis that tents offer rich light conditions by partly allowing sunlight to pass through the leaves and this makes that yellow coloration probably provides camouflage benefits to tent-roosting bats, that gregariousness facilitates visual communication, and that all Stenodermatinae bats possess retinal L-cones that allow the perception of long-wavelength light and have a frugivorous diet from which carotenoids are obtained, we hypothesized that tent-roosting may have driven the evolution of yellow skin coloration in this group of bats. We tested this prediction in 71 species within Stenodermatinae. Reconstructions of ancestral states showed that the common ancestor was most likely not colorful and did not roost in tents, but both traits early appeared in the first phylogenetic ramification. Phylogenetically controlled analyses showed that, as predicted, yellow skin coloration and tent-roosting coevolved after their appearance. This is the first explanation for the evolution of body coloration in nocturnal mammals. As the light environment of nocturnal forests is dominated by yellow-green wavelengths that coincide with the spectral sensitivity of some bats, nocturnal light conditions may have acted jointly with diurnal light conditions in tents to favor the evolution of yellow skin coloration in these animals.