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Acute sensitivity to interaural time differences in the inferior colliculus of a bat that relies on passive sound localization.

Gleaning bats rely on passive hearing to detect and localize terrestrial prey, and display remarkable accuracy in their passive sound localization. This study examines binaural processing in the inferior colliculus (IC) of the pallid bat (Antrozous pallidus), a gleaner that attends to prey-generated noise transients to locate prey. The primary focus is to determine whether neurons in its lateral IC, a region that appears dedicated to passive localization, possess a level of sensitivity to interaural time difference (ITD) sensitivity sufficient to indicate the use of ITDs in sound localization. Such a sensitivity was suspected because the pallid bat is capable of very accurate passive sound localization at the lower end of its audible range, where interaural intensity differences (IIDs) are small and may not provide sufficient spatial information. Because the pallid bat's audible range is too high for neurons to phase-lock to carrier frequencies, neurons were tested with square-wave, amplitude-modulated tones and noise to determine their sensitivity to ITDs in the sound envelope. Their sensitivity to the bat's behaviorally relevant ITD range of +/- 70 micros, and their low average interaural time/ intensity trading ratios (18 micros/dB) suggest that the pallid bat IC may have the greatest ITD sensitivity reported in a high-frequency mammalian auditory system.

Acoustic Stimulation↗

Phylogenetic diversity of bat trypanosomes of subgenus Schizotrypanum based on multilocus enzyme electrophoresis, random amplified polymorphic DNA, and cytochrome b nucleotide sequence analyses.

Trypanosome stocks isolated from bats (Chiroptera) and belonging to the subgenus Schizotrypanum were analyzed by multilocus enzyme electrophoresis (MLEE) at 22 loci, random amplified polymorphic DNA (RAPD) with 14 primers and/or cytochrome b nucleotide sequence. Bat trypanosomes belonged to the species Trypanosoma cruzi marinkellei (10 stocks), Trypanosoma dionisii (four stocks) and Trypanosoma vespertilionis (three stocks). One T. rangeli stock and seven stocks of T. cruzi sensu stricto, the agent of Chagas disease, were included for comparison. The homology of several RAPD fragments shared by distinct species was verified by hybridization. The sequence of a 516-nucleotide portion of the maxicircle-encoded cytochrome b (CYb) coding region was determined in representative stocks of the species under study. Phylogenetic analysis of the data confirmed the previous taxonomic attribution of these bat trypanosomes based on biological, epidemiological and ecological features. However, a new finding was that within T. cruzi marinkellei two major subdivisions could be distinguished, T.c.m. I, found in the spear-nose bats Phyllostomus discolor and Phyllostomus hastatus, and T.c.m. II, from P. discolor. In addition, the T. c. marinkellei 'Z' stock from a short-tailed bat (Carollia perspicillata) was distantly related to these two subdivisions, and the monophyly of T. c. marinkellei is unclear based on the present data. Based on the present sample, the European species T. dionisii and T. vespertilionis appeared to be more homogeneous. RAPD and CYb data both suggested the monophyly of a group composed of T. cruzi and the two major subdivisions of T. cruzi marinkellei. This study shows that MLEE, RAPD and CYb can be used for taxonomic assignment and provide valuable phylogenetic information for strains and taxa within the subgenus Schizotrypanum. An evolutionary scenario in which the broad host-range parasite T. cruzi would be derived from a bat-restricted trypanosome ancestor is discussed.

Animals↗

Seeing in the dark: molecular approaches to the study of bat populations.

Whilst the use of molecular genetic techniques is widespread in the fields of population and evolutionary biology, their application within the mammalian order Chiroptera neither reflects the species richness nor the ecological and behavioural diversity of the order. This is despite the fact that the Chiroptera are problematic to study using more direct observational techniques. Here, we standardize and synthesise the current data, assess the contribution of molecular research to the study of bat species and highlight the importance of its continued and expanded use. At an inter-population level, molecular studies have demonstrated a great diversity of population genetic structure within the order. Among populations of migratory species, genetic structure appears universally low, and hence seasonal movement is likely to be the prevailing influence. However, for sedentary species an array of factors including dispersal ability, extrinsic barriers to gene flow and historical events may determine the extent of genetic partitioning among populations. Intrinsic factors such as wing morphology or roost requirements may also influence population genetic structure in sedentary bat species, a proposal which requires further research. Molecular studies have also made important contributions towards an understanding of social organisation in bats. Evidence indicates that in many polygynous species male mating success does not translate directly into reproductive success, perhaps as a result of multiple mating by females. Estimates of relatedness within and genetic structure among colonies are, in general, very low; a finding which has important implications regarding theories concerning the formation and persistence of bat social groups. Molecular studies have provided new and important insights into the ecology of bats, and have opened up exciting and previously unexplored avenues of research. The data from these studies suggest not only a predictive framework for future studies, but also the use of genetic data in the management and conservation of bat species.

Animal Migration↗

A phylogenetic supertree of the bats (Mammalia: Chiroptera).

We present the first estimate of the phylogenetic relationships among all 916 extant and nine recently extinct species of bats Mammalia: Chiroptera), a group that accounts for almost one-quarter of extant mammalian diversity. This phylogeny was derived by combining 105 estimates of bat phylogenetic relationships published since 1970 using the supertree construction technique of Matrix Representation with Parsimony (MRP). Despite the explosive growth in the number of phylogenetic studies of bats since 1990, phylogenetic relationships in the order have been studied non-randomly. For example, over one-third of all bat systematic studies to date have locused on relationships within Phyllostomidae, whereas relationships within clades such as Kerivoulinae and Murinae have never been studied using cladistic methods. Resolution in the supertree similarly differs among clades: overall resolution is poor (46.4%, of a fully bifurcating solution) but reaches 100% in some groups (e.g. relationships within Mormoopidae). The supertree analysis does not support a recent proposal that Microchiroptera is paraphyletic with respect to Megachiroptera, as the majority of source topologies support microbat monophyly. Although it is not a substitute for comprehensive phylogenetic analyses of primary molecular and morphological data, the bat supertree provides a useful tool for future phylogenetic comparative and macroevolutionary studies. Additionally, it identifies clades that have been little studied, highlights groups within which relationships are controversial, and like all phylogenetic studies, provides preliminary hypotheses that can form starting points for future phylogenetic studies of bats.

Animals↗

Ageing studies on bats: a review.

Bat biologists have long known about the exceptional longevity of bats (Order: Chiroptera), which is unusual for mammals of such a small size and a high metabolic rate. Yet relatively few mechanistic studies have focused on this longevity. On average, species of Chiroptera live three times longer than predicted by their body size. In addition, bats have other life history traits that are characteristic of large, long-lived mammals such as few and large offspring and slow growth rates. Bats fit the evolutionary theory of ageing, as their extended longevity is predicted by their ability to escape extrinsic mortality through flight and, in some species, hibernation. They also show tradeoffs between longevity and reproduction, as predicted by the disposable soma theory of ageing. From a physiological perspective, bat longevity reportedly correlates with replicative longevity, low brain calpain activity, and reduced reactive oxygen species production. As long-lived and physiologically interesting organisms, bats may prove to be an informative model system for ageing research.

Age Factors↗

Classification of virtual objects in the echolocating bat, Megaderma lyra.

Using echolocation, bats can not only locate objects in space but also discriminate objects of different shape. The acoustic image of an object is its impulse response (IR). The current experiments investigate whether bats just perceive changes in echo composition or whether bats perceive the IR itself through a detailed comparison of the emitted sound with the echo. The bat Megaderma lyra was trained to classify unknown virtual objects according to learned reference objects of different temporal and spectral composition. The bats' spontaneous classification was compared to predictions based on variousphysical and simulated peripheral auditory representations of the objects. The results show that the bats developed an accurate internal representation of the objects' IRs. In the auditory periphery, the IRs of small objects (< 4-6 cm) are coded along the tonotopic frequency axis.

Acoustics↗

Evidence for a spectral basis of texture perception in bat sonar.

Bats obtain information about the structure of objects in the outside world from their echolocation signals, an extremely useful method when hunting non-flying prey in densely cluttered habitats, for example. Information about object structure is contained both in the time and in the spectral interference patterns of signals reflected from surfaces at different distances from the bat. I report here an experiment designed to test the extent to which bats use these two types of information. A 'phantom target' is generated by playing back to an echolocating bat signals that mimic the result of reflection from two planes set at different distances. The ability of the bat to discriminate between two such targets is investigated as a function of the separations of the planes. Several of the results do not fit the hypothesis that the bat simply uses time-delay information: the very small time difference that can be discriminated, the fall off in ability to discriminate planes at a particular separation and the symmetry of the discrimination ability measured in the frequency domain. The empirical data can best be fitted by a function based on spectral correlation.

Animals↗

Nectar bat stows huge tongue in its rib cage.

Bats of the subfamily Glossophaginae (family Phyllostomidae) are arguably the most specialized of mammalian nectarivores, and hundreds of neotropical plants rely on them for pollination. But flowers pollinated by bats are not known to specialize for bat subgroups (unlike flowers that have adapted to the length and curvature of hummingbird bills, for example), possibly because the mouthparts of bats do not vary much compared with the bills of birds or the probosces of insects. Here I report a spectacular exception: a recently-described nectar bat that can extend its tongue twice as far as those of related bats and is the sole pollinator of a plant with corolla tubes of matching length.

Animals↗

The comparative phylogeography of neotropical mammals: patterns of intraspecific mitochondrial DNA variation among bats contrasted to nonvolant small mammals.

The major aim of this study was to compare the phylogeographic patterns of codistributed bats and small nonvolant Neotropical mammals. Cytochrome b sequences (mitochondrial DNA) were obtained for a total of 275 bats representing 17 species. The tissue samples were collected in coastal Brazil, and were available from Mexico and the Guyana. The study concentrates on four species (Artibeus lituratus, Carollia perspicillata, Sturnira lilium and Glossophaga soricina) which were well represented. The other 13 species were sequenced to test the generality of the patterns observed. In general, sequence divergence values within species were low, with most bat species presenting less than 4% average sequence divergence, and usually between 1 and 2.5%. Clades of highly similar haplotypes enjoyed broad distribution on a continental scale. These clades were not usually geographically structured, and at a given locality the number of haplotypes was high (8-10). As distance increased, some moderately divergent clades were found, although the levels of divergence were low. This suggests a geographical effect that varied depending on species and scale. Small nonvolant mammals almost invariably have high levels of sequence divergence (> 10%) for cytochrome b over much shorter distances (< 1000 km). The grain of intraspecific variation found in small nonvolant mammals is much finer than in bats. Low levels of geographical structuring cannot be attributed to a slower evolutionary rate of bat DNA in relation to other mammalian taxa. The phylogeographic pattern of bats contrasts sharply with the pattern found for Neotropical rodents and marsupials.

Animals↗

Delay accuracy in bat sonar is related to the reciprocal of normalized echo bandwidth, or Q.

Big brown bats (Eptesicus fuscus) emit wideband, frequency-modulated biosonar sounds and perceive the distance to objects from the delay of echoes. Bats remember delays and patterns of delay from one broadcast to the next, and they may rely on delays to perceive target scenes. While emitting a series of broadcasts, they can detect very small changes in delay based on their estimates of delay for successive echoes, which are derived from an auditory time/frequency representation of frequency-modulated sounds. To understand how bats perceive objects, we need to know how information distributed across the time/frequency surface is brought together to estimate delay. To assess this transformation, we measured how alteration of the frequency content of echoes affects the sharpness of the bat's delay estimates from the distribution of errors in a psychophysical task for detecting changes in delay. For unrestricted echo frequency content and high echo signal-to-noise ratio, bats can detect extremely small changes in delay of about 10 ns. When echo bandwidth is restricted by filtering out low or high frequencies, the bat's delay acuity declines in relation to the reciprocal of relative echo bandwidth, expressed as Q, which also is the relative width of the target impulse response in cycles rather than time. This normalized-time dimension may be efficient for target classification if it leads to target shape being displayed independent of size. This relation may originate from cochlear transduction by parallel frequency channels with active amplification, which creates the auditory time/frequency representation itself.

Animals↗

Histological convergent evolution of the accessory submandibular glands in four species of frog-eating bats.

The accessory submandibular glands in four species of bats were examined by electron microscopy. These four species represent two independently evolved lineages. The fringe-lipped bat, Trachops cirrhosis, is a Neotropical phyllostomid species, whereas the false vampire bats of southeast Asia, Megaderma lyra and M. spasma, and the heart-nosed bat, Cardioderma cor, of East Africa are megadermatid species. These glands show extreme deviation from typical salivary gland histology: their secretory endpieces are in the form of follicles and their ducts lack the cytological details that permit identification of diverse duct segments. Despite their unusual histology, the secretory endpieces in M. lyra, M. spasma, and C. cor consist of secretory cells that conform to typical secretory cell morphology. In contrast, secretion by follicular cells in T. cirrhosis involves unusual cytoplasmic bodies, and their mitochondria frequently have intracristal crystalloids. Ducts in all four species consist of simple cuboidal to columnar epithelium without basal striations. Follicles and ducts in all four bats are surrounded by numerous myoepithelial cells and are heavily innervated by hypolemmal nerve terminals. Despite their widely separated geographical ranges, all four bat species consume frogs and other vertebrates. Frogs and toads often possess toxic cutaneous glands that provide a chemical defense against predation. It is postulated that the unusual accessory glands in the four frog-eating species secrete toxin-neutralizing salivary factors. The follicular form of the endpieces permits storage of preformed saliva and their coterie of myoepithelial cells and hypolemmal nerve terminals facilitates the sudden and rapid expulsion of saliva into the oral cavity during the consumption of noxious amphibians.

Animals↗

An impact analysis of a flexible bat using an iterative solver.

Although technology has now infiltrated and prompted evolution in most mass participation sports, the advances in bat technology in such sports as baseball and cricket have been relatively minor. In this study, we used a simple finite element modelling approach to try to shed new light upon the underlying mechanics of the bat-ball impact, with a view to the future optimization of bat design. The analysis of a flexible bat showed that the point of impact that produced the maximum post-impact ball velocity was a function of the bat's vibrational properties and was not necessarily at the centre of percussion. The details of the analysis agreed well with traditional Hertzian impact theory, and broadly with empirical data. An inspection of the relative modal contributions to the deformations during impact also showed that the position of the node of the first flexure mode was important. In conclusion, considerable importance should be attached to the bat's vibrational properties in future design and analysis.

Baseball↗

Studies on the pathogenesis of rabies in insectivorous bats. I. Role of brown adipose tissue.

Studies on the pathogenesis of rabies in two species of experimentally infected insectivorous Chiroptera, the Mexican free-tailed bat (Tadarida mexicana), a quasi hibernator, and the little brown bat (Myotis lucifugus), a deep hibernator, provided evidence that brown adipose tissue may serve as an extraneural site for storage and multiplication of rabies virus. Although the Mexican free-tailed bat proved to be relatively insusceptible to experimental rabies infection, virus was demonstrated in the brown fat of 22 per cent of those animals shown to be infected by viral assay in white Swiss mice. Rabies infection in this species was most evident 20 to 40 days after intramuscular inoculation of virus. Rabies virus was found to be widely distributed in the little brown myotis 9 to 26 days following inoculation and virus concentrations in some of the tissues approached the level of the stock mouse brain virus suspension used in inoculating these bats. The shorter incubation period and higher virus titers in the tissues assayed reflect the increased susceptibility of Myotis lucifugus as compared with the Mexican free-tailed bat. Virus was demonstrated in the brown fat of 30 per cent of the experimentally infected Myotis. In the experimentally infected Myotis lucifugus and in the Syrian hamster which is highly susceptible to rabies infection, rabies virus was isolated more frequently from the brown fat than from the salivary gland indicating that in a susceptible host brown adipose tissue may be as frequent a site of viral proliferation as salivary gland. Since rabies virus was found to persist for long periods of time in the brown fat of experimentally infected bats and was occasionally demonstrated in this tissue alone, it is suggested that brown adipose tissue provides a mechanism by which these animals may serve as reservoirs for this agent in nature. The possibility that similar mechanisms may be involved in the maintenance of other viral agents during interepidemic periods is discussed.

Adipose Tissue↗

Biological correlates of extinction risk in bats.

We investigated patterns and processes of extinction and threat in bats using a multivariate phylogenetic comparative approach. Of nearly 1,000 species worldwide, 239 are considered threatened by the International Union for Conservation of Nature and Natural Resources (IUCN) and 12 are extinct. Small geographic ranges and low wing aspect ratios are independently found to predict extinction risk in bats, which explains 48% of the total variance in IUCN assessments of threat. The pattern and correlates of extinction risk in the two bat suborders are significantly different. A higher proportion (4%) of megachiropteran species have gone extinct in the last 500 years than microchiropteran bats (0.3%), and a higher proportion is currently at risk of extinction (Megachiroptera: 34%; Microchiroptera: 22%). While correlates of microchiropteran extinction risk are the same as in the order as a whole, megachiropteran extinction is correlated more with reproductive rate and less with wing morphology. Bat extinction risk is not randomly distributed phylogenetically: closely related species have more similar levels of threat than would be expected if extinction risk were random. Given the unbalanced nature of the evolutionary diversification of bats, it is probable that the amount of phylogenetic diversity lost if currently threatened taxa disappear may be greater than in other clades with numerically more threatened species.

Animals↗

Fatal human rabies caused by European bat Lyssavirus type 2a infection in Scotland.

We wish to report the first recorded case of indigenous human rabies caused by a bat bite in the United Kingdom in 100 years. This instructive case report highlights a number of key lessons: first, bites from insectivorous bats indiginous to the United Kingdom can cause rabies in humans; second, rabies immunization is essential for bat-handlers, and postexposure treatment for rabies is essential for patients bitten by bats; third, patients able to give a history who present with acute flaccid paralysis and/or presumptive viral encephalitis should be asked if they have been bitten by bats, irrespective of travel history, or this history should be obtained from family or friends; fourth, antemortem diagnosis of bat rabies (EBLV type 2a infection) in humans is possible using RT-PCR.

Animals↗

Natural use of heterothermy by a small, tree-roosting bat during summer.

Little is known about the use of heterothermy by wild bats during summer, especially for tree-roosting species. Because thermal conditions within tree roosts can fluctuate widely with ambient temperature, which affects thermoregulatory energy expenditure during diurnal roosting, we measured skin temperatures of free-ranging male Nyctophilus geoffroyi (8 g) to quantify the relation between summer torpor use and roost thermal conditions. Bats roosted under bark on the northern (sunny) side of trees and entered torpor every day, usually near sunrise. Bats exhibited two bouts of torpor on most days: the first occurred in the morning, was terminated by partially passive rewarming, and was followed by a period of normothermy during the warmest part of the day; a second torpor bout occurred in the late afternoon, with arousal near sunset. On the warmest days, bats had only a single, short morning bout. On the coolest days, bats remained torpid throughout the day, and one 2-d bout was observed. Thus, presumably owing to their poorly insulated roosts and the high energetic cost of normothermy at temperatures below 30 degrees C, the extent and timing of heterothermy was closely related to the cycle of diurnal temperatures. Our study indicates that torpor use is important for energy maintenance during summer diurnal roosting of N. geoffroyi and likely of other small, tree-roosting bats.

Animals↗

Physiological constraint to food ingestion in a new world nectarivorous bat.

We investigated the intake response of the nectarivorous Pallas's long-tongued bat Glossophaga soricina to different nectar concentrations to test the hypothesis that bats show compensatory feeding. Bats were offered sucrose solutions between 146 and 1,168 mmol L(-1). Contrary to our expectations, long-tongued bats did not show compensatory feeding, suggesting that volumetric food intake is physiologically constrained. Energy intake was lower at the most dilute solutions (146-584 mmol L(-1)) and then remained relatively constant at more concentrated diets (876 and 1,168 mmol L(-1)). The shape of the observed intake response was very similar to the one predicted by a model dependent on intestinal morphology and in vitro sucrase activity. However, the model predicted higher volumetric food intake at the lower concentrations tested, which suggests that the intestines of the bats were not functioning to their full capacity. Rates of sucrose hydrolysis and water processing probably constrain food intake in long-tongued bats as diets get more dilute.

Analysis of Variance↗

Fatal encephalitis caused by a bat-borne rabies-related virus. Clinical findings.

The clinical findings are described in the first reported European case of fatal encephalitis of bat origin caused by a rabies-related virus. A bat zoologist developed the symptoms of rabies 51 days after his last exposure to a bat bite. The clinical disease of 23 days duration was a combination of the paralytic and 'furious' forms of rabies. Serial BAEP and EEG recordings, CT and MR scans of the brain, as well as CSF findings, demonstrated severe ascending destruction of the brain. An unusual progression from isolated brainstem death to cortical brain death occurred. Neuropathologically, the brain showed severe lytic changes. The presence of rabies-related virus antigens in brain smears was shown using a panel of fluorescent antibodies. The virus was inoculated into and isolated from suckling mice. The virus had a close resemblance to European bat rabies isolates, which belong to the group of rabies-related viruses. Of particular concern is whether the virus can spread from bats to terrestrial animals and whether the European type of bat rabies constitutes a danger to man.

Adult↗