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Group decision making in fission-fusion societies: evidence from two-field experiments in Bechstein's bats.

Group decisions are required when group coordination is beneficial, but individuals can choose between alternatives. Despite the increased interest in animal group decision making, there is a lack of experimental field studies that investigate how animals with conflicting information make group decisions. In particular, no field studies have considered the influence of fission-fusion behaviour (temporary splitting into subgroups) on group decisions. We studied group decision making in two wild Bechstein's bat colonies, which are fission-fusion societies of stable individual composition. Since they frequently switch communal roosts, colony members must regularly make group decisions over where to roost. In the two-field experiments, we provided marked individuals with conflicting information about the suitability of potential roosts. We investigated whether conflicting information led to group decisions that followed a 'unanimous' or a 'majority' rule, or increased colony fission. Individual behaviour suggests that bats considered both their own information and the behaviour of others when deciding where to roost. Group decisions about communal roosts reflected the information available to a majority of the bats roosting together, but conflicting information led to an increased fission in one colony. Our results suggest that fission-fusion societies allow individuals to avoid majority decisions that are not in their favour.

Animals↗

Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores.

How brains have evolved in response to particular selection pressures is illuminated by ecological correlates of differences in brain structure among contemporary species. The focus of most comparative studies has been on the overall size of brains relative to body size, hence ignoring the ways in which selection operates on specific neural systems. Here we investigate evolutionary radiations in the size of visual and olfactory brain structures within three orders of mammals: primates, bats and insectivores. The comparative relationships within these three orders show both similarities and differences. After removal of the allometric effect of overall brain size, the sizes of different structures within each sensory modality are positively correlated in all three orders. Correlations between visual and olfactory structures, however, are negative in primates, negative but non-significant in insectivores, and positive in bats. In both primates and insectivores, nocturnal lineages tend to have larger olfactory structures than do diurnal or partly diurnal lineages, and among the primates diurnal lineages have larger striate visual cortexes. Hence the apparent trade-off between vision and olfaction in primates seems to be related to the divergence of nocturnal and diurnal forms. However, negative correlations between visual and olfactory structures were also found when nocturnal strepsirhines and diurnal haplorhines were analysed separately, suggesting that ecological variables in addition to activity timing may be significant. Indeed, there were also associations with diet: frugivory was associated with enlargements of the geniculostriate visual system in diurnal primates, enlargements of olfactory structures in nocturnal primates, and possibly enlargements of both in bats. Further ecological associations were found within insectivores: aquatic lineages had smaller olfactory structures than in their non-aquatic counterparts, and fossorial lineages had smaller optic nerves than in non-fossorial forms. We conclude that activity timing, diet and habitat have each played a role in the evolutionary radiation of mammalian sensory systems, but with varying effects in the different taxa. Some of the associations between ecology and sensory systems suggest alternative explanations for correlates of overall brain size, which have in the past commonly been interpreted in terms of selection on intelligence.

Adaptation, Biological↗

Base-compositional biases and the bat problem. II. DNA-hybridization trees based on AT- and GC-enriched tracers.

We conducted a series of parallel DNA-hybridization experiments on a small group of bats (species of Pteropus, Rhinolophus, Noctilio and Pteronotus) and outgroups (Lemur, Cynocephalus, Didelphis), using whole-genome labels and tracers made from extracts enriched with AT and two levels of GC content. FITCH (additive phylogenetic trees) topologies were constructed from the four sets of comparisons, indexed as both delta Tmode and delta NPHs (normalized percentage of hybridization). Based on our previous work showing that the shared AT bias of pteropodids and some microchiropterans may affect the rank-ordering of taxa based on either AT- or GC-rich labels, our expectation was that the resulting trees would show differing topologies when generated from tracers made with the variously enriched DNA extracts. Whereas there was some variation among the trees, most of them grouped the bats together, and almost all paired the representative megachiropteran and rhinolophoid microchiropteran as sister-taxa in contrast to the other microchiropterans. As the pteropodid-rhinolophoid relationship is an unexpected and unlikely one, we attribute this association to an AT bias that was not obviated even by our most GC-rich labels, and suggest that such a bias may compromise the truth of some molecular trees. Accordingly, we believe the broader issue of bat monophyly remains unresolved by DNA-hybridization and probably also by gene-sequencing studies.

Animals↗

Isolation of Hendra virus from pteropid bats: a natural reservoir of Hendra virus.

Since it was first described in Australia in 1994, Hendra virus (HeV) has caused two outbreaks of fatal disease in horses and humans, and an isolated fatal horse case. Our preliminary studies revealed a high prevalence of neutralizing antibodies to HeV in bats of the genus PTEROPUS:, but it was unclear whether this was due to infection with HeV or a related virus. We developed the hypothesis that HeV excretion from bats might be related to the birthing process and we targeted the reproductive tract for virus isolation. Three virus isolates were obtained from the uterine fluid and a pool of foetal lung and liver from one grey-headed flying-fox (Pteropus poliocephalus), and from the foetal lung of one black flying-fox (P. alecto). Antigenically, these isolates appeared to be closely related to HeV, returning positive results on immunofluorescent antibody staining and constant-serum varying-virus neutralization tests. Using an HeV-specific oligonucleotide primer pair, genomic sequences of the isolates were amplified. Sequencing of 200 nucleotides in the matrix gene identified that these three isolates were identical to HeV. Isolations were confirmed after RNA extracted from original material was positive for HeV RNA when screened on an HeV Taqman assay. The isolation of HeV from pteropid bats corroborates our earlier serological and epidemiological evidence that they are a natural reservoir host of the virus.

Animals↗

A molecular epidemiological study of Australian bat lyssavirus.

The genetic diversity of Australian bat lyssavirus (ABL) was investigated by comparing 24 ABL isolate glycoprotein (G) gene nucleotide sequences with those of 37 lyssaviruses representing Lyssavirus genotypes 1-6. Phylogenetic analyses indicated that ABL forms a monophyletic group separate from other lyssaviruses. This group differentiates into two clades: one associated with Pteropus (flying fox) species, the other with the insectivorous bat Saccolaimus flaviventris. Calculation of percentage nucleotide identities between isolates of the two clades revealed up to 18.7 % nucleotide sequence divergence between the two ABL variants. These observations suggest that ABL is a separate lyssavirus species with a similar epidemiology to chiropteran rabies virus (RV), where two distinct ABL variants co-exist in Australia in bat species with dissimilar ecology. Analyses of selection pressures in ABL G gene sequences provided some evidence of weak positive selection within the endodomain at amino acids 499 and 501, although in general the dominant evolutionary process observed was purifying selection. This intimates that, in nature, isolates of ABL, like those of RV, are subject to relatively strong selective constraints, suggesting a stability of host species, cell tropisms and ecological conditions.

Amino Acid Sequence↗

Molecular epidemiology of rabies epizootics in Colombia: evidence for human and dog rabies associated with bats.

Three urban rabies outbreaks have been reported in Colombia during the last two decades, one of these is occurring in the Caribbean Region (northern Colombia), while the other two occurred almost simultaneously in Arauca (eastern Colombia) and in the Central Region and ended in 1997. In order to derive phylogenetic relationships between rabies viruses isolated in these three areas, 902 nt cDNA fragments encoding the cytoplasmic domain of protein G and a fragment of protein L were obtained by RT-PCR. These amplicons contained the G-L intergenic region and were sequenced to draw phylogenetic trees. Phylogenetic analysis showed three distinct groups of viruses in the study sample. Colombian genetic variant I viruses were isolated in both Arauca and the Central Region. These viruses are apparently extinct in Colombia. Colombian genetic variant II viruses were isolated in the Caribbean Region and are still being transmitted in that area. The third group of viruses consists of viruses isolated from two insectivorous bats, three domestic dogs and a human. According to sequence analysis, the data here indicate that the isolates in this third group are bat rabies virus variants. This finding is the first that associates bats to rabies in Colombian dogs and humans, showing an unsuspected vector threatening animal and public health.

Amino Acid Sequence↗

Noseleaf furrows in a horseshoe bat act as resonance cavities shaping the biosonar beam.

Horseshoe bats emit their ultrasonic biosonar pulses through nostrils surrounded by intricately shaped protuberances (noseleaves). While these noseleaves have been hypothesized to affect the sonar beam, their physical function has never been analyzed. Using numerical methods, we show that conspicuous furrows in the noseleaf act as resonance cavities shaping the sonar beam. This demonstrates that (a) animals can use resonances in external, half-open cavities to direct sound emissions, (b) structural detail in the faces of bats can have acoustic effects even if it is not adjacent to the emission sites, and (c) specializations in the biosonar system of horseshoe bats allow for differential processing of subbands of the pulse in the acoustic domain.

Acoustics↗

"Markov at the bat": a model of cognitive processing in baseball batters.

Anecdotal evidence from players and coaches indicates that cognitive processing (e.g., expectations about the upcoming pitch) plays an important role in successful baseball batting, yet this aspect of hitting has not been investigated in detail. The present study provides experimental evidence that prior expectations significantly influence the timing of a baseball swing. A two-state Markov model was used to predict the effects of pitch sequence and pitch count on batting performance. The model is a hitting strategy of switching between expectancy states using a simple set of transition rules. In a simulated batting experiment, the model provided a good fit to the hitting performance of 6 experienced college baseball players, and the estimated model parameters were highly correlated with playing level.

Adult↗

Mitochondrial DNA variation and population structure of the island endemic Azorean bat (Nyctalus azoreum).

The Azorean bat Nyctalus azoreum is the only endemic mammal native to the remote archipelago of the Azores. It evolved from a continental ancestor related to the Leisler's bat Nyctalus leisleri and is considered threatened because of its restricted and highly fragmented distribution. We studied the genetic variability in 159 individuals from 14 colonies sampled throughout the archipelago. Sequences of the D-loop region revealed moderate but highly structured genetic variability. Half of the 15 distinct haplotypes were restricted to a single island, but the most common was found throughout the archipelago, suggesting a single colonization event followed by limited interisland female gene flow. All N. azoreum haplotypes were closely related and formed a star-like structure typical of expanded populations. The inferred age of demographic expansions was consistent with the arrival of founder animals during the Holocene, well before the first humans inhabited the Azores. Comparisons with a population of N. leisleri from continental Portugal confirmed not only that all N. azoreum lineages were unique to the archipelago, but also that the current levels of genetic diversity were surprisingly high for an insular species. Our data imply that the Azorean bat has a high conservation value. We argue that geographical patterns of genetic structuring indicate the existence of two management units.

Animals↗

A tale of two siblings: multiple paternity in big brown bats (Eptesicus fuscus) demonstrated using microsatellite markers.

In many bat species, the opportunity for sperm competition or other mechanisms of post-copulatory paternity biasing is thought to be great, due to the long delay between copulation and fertilization, demonstrated sperm storage capabilities, and observed promiscuity. We present the results of the first study to assess whether litters of big brown bats (Eptesicus fuscus) containing dizygotic twins share the same father. We sampled 26 mother-offspring triads from three colonies in Indiana and Illinois, as well as 299 additional adults (237 females and 62 males) from these colonies and six other maternity colonies in the same area in 1997-1998. All individuals were genotyped at nine highly variable autosomal microsatellite loci and one X-linked locus. We assessed multiple paternity using autosomal and X-linked locus exclusions, and using maximum-likelihood methods. All methods confirmed multiple paternity within litters, and the maximum-likelihood analyses indicated that almost half of the sampled litters were composed of maternal half-siblings rather than full-siblings. Our results highlight the potential importance of post-copulatory mechanisms of paternity determination in the mating system of big brown bats, and have important implications for gene flow and population structuring in this species.

Animals↗

Echolocation performance of the vampire bat (Desmodus rotundus).

The neotropical vampire bats (Desmodus rotundus) echolocate using ultrasonic pulses like those of the Latin American phyllostomatid bats. In this paper the orally produced echolocation sounds of Desmodus are analysed and the performance of the echolocation system is studied in two-choice training experiments on two vampire bats. Ability to detect objects is relatively limited; both animals were capable of discerning the presence of a 1 cm wide metal strip at a distance of 50 cm, but they failed with 0.5 cm wide strips. The ultrasonic pulses produced at a distance of 50 cm appear to sample an area with a diameter of 2.5 to 3.0 cm (i.e., the solid angle tested with each pulse is 3 degrees to 3 degrees 40' in extent).

Animals↗

Auditory cortex of the rufous horseshoe bat: 1. Physiological response properties to acoustic stimuli and vocalizations and the topographical distribution of neurons.

The extent and functional subdivisions of the auditory cortex in the echolocating horseshoe bat, Rhinolophus rouxi, were neurophysiologically investigated and compared to neuroarchitectural boundaries and projection fields from connectional investigations. The primary auditory field shows clear tonotopic organization with best frequencies increasing in the caudorostral direction. The frequencies near the bat's resting frequency are largely over-represented, occupying six to 12 times more neural space per kHz than in the lower frequency range. Adjacent to the rostral high-frequency portion of the primary cortical field, a second tonotopically organized field extends dorsally with decreasing best frequencies. Because of the reversed tonotopic gradient and the consistent responses of the neurons, the field is comparable to the anterior auditory field in other mammals. A third tonotopic trend for medium and low best frequencies is found dorsal to the caudal primary field. This area is considered to correspond to the dorsoposterior field in other mammals. Cortical neurons had different response properties and often preferences for distinct stimulus types. Narrowly tuned neurons (Q10dB > 20) were found in the rostral portion of the primary field, the anterior auditory field and in the posterior dorsal field. Neurons with double-peaked tuning curves were absent in the primary area, but occurred throughout the dorsal fields. Vocalization elicited most effectively neurons in the anterior auditory field. Exclusive response to pure tones was found in neurons of the rostral dorsal field. Neurons preferring sinusoidal frequency modulations were located in the primary field and the anterior and posterior dorsal fields adjacent to the primary area. Linear frequency modulations optimally activated only neurons of the dorsal part of the dorsal field. Noise-selective neurons were found in the dorsal fields bordering the primary area and the extreme caudal edge of the primary field. The data provide a survey of the functional organization of the horseshoe bat's auditory cortex in real coordinates with the support of cytoarchitectural boundaries and connectional data.

Acoustic Stimulation↗

Inhibitory effects of melatonin on testosterone but not on androstenedione production during winter in the vespertilionid bat, Scotophilus heathi.

The possible effects of melatonin on testosterone and androstenedione production in vitro by testes of wild-caught bats, Scotophilus heathi, during different reproductive phases were investigated. Bats were captured during reproductive quiescent (April-August), recrudescent (September-October), breeding (November-February), and winter dormancy (late December-January) phases. Testes were incubated in media-199 for 2 h at 37 degrees C with luteinizing hormone (LH) and with or without melatonin. Melatonin had no effect on LH-induced testosterone (T) or androstenedione (A) production during the quiescent, recrudescent, and breeding phases. However, it significantly (P < 0.05) suppressed LH-induced T production but had no effect on A during winter dormancy. Testicular 17 beta-hydroxy steroid dehydrogenase (17 beta-HSD) activity was then measured in the testes from bats trapped during quiescence, breeding, and winter dormancy. Interestingly, melatonin along with LH caused suppression of 17 beta-HSD activities (3.56 +/- 0.03 unit/min/mg protein) when compared with levels of LH treated testes (7.10 +/- 1.15 unit/min/mg protein) during winter dormancy, while it had no significant effect on 17 beta-HSD activity during quiescence and breeding phases. These results suggest that in S. heathi, melatonin during winter dormancy suppresses LH-induced T production by the testes via the suppression of 17 beta-HSD activity. This may be the reason for the decline in testicular activity during winter dormancy.

17-Hydroxysteroid Dehydrogenases↗

[An outbreak of acute pulmonary histoplasmosis among travelers to a bat-inhabited cave in Brazil].

Histoplasmosis is known to be endemic in various parts of the world, especially in North and Latin America. In Japan, Histoplasma capsulatum has rarely been isolated from the natural environment. To date, only seven cases of histoplasmosis have been reported in Japan including some that were contracted in foreign countries. Herein, we report the occurrence of acute histoplasmosis among Japanese travelers who were exposed to bat guano in a cave near Manaus, Brazil. A group of 8 Japanese travelers entered a cave for a total of 2 hours in March, 1993. All the visitors had been healthy and had no history of abnormal chest roentgenograms. From 10 to 20 days after the exposure, 7 (87.5%) of the 8 individuals developed abnormal symptoms including fever, malaise, loss of appetite, myalgia, arthralgia, chest pain and dry cough. Five (62.5%) had nodular infiltrative shadows with or without hilar lymphadenopathy in the chest roentgenograms. Eight (100%) of the individuals showed serologic evidence of histoplasmosis. Despite the small number of subjects, this high rate of infection may be related to the fact that the subjects stayed in an enclosed area where air exchange was minimal, at the end of a deep cave infested with numerous bats. The cave involved has never been documented as being endemic for histoplasmosis. The threat of H. capsulatum infection in bat-inhabited caves should be emphasized to travelers and also to physicians.

Adult↗

A computational sensorimotor model of bat echolocation.

A computational sensorimotor model of target capture behavior by the echolocating bat, Eptesicus fuscus, was developed to understand the detection, localization, tracking, and interception of insect prey in a biological sonar system. This model incorporated acoustics, target localization processes, flight aerodynamics, and target capture planning to produce model trajectories replicating those observed in behavioral insect capture trials. Estimates of target range were based on echo delay, azimuth on the relative intensity of the echo at the two ears, and elevation on the spectral pattern of the sonar return in a match/mismatch process. Flapping flight aerodynamics was used to produce realistic model trajectories. Localization in all three spatial dimensions proved necessary to control target tracking and interception for an adequate model of insect capture behavior by echolocating bats. Target capture using maneuvering flight was generally successful when the model's path was controlled by a planning process that made use of an anticipatory internal simulation, while simple homing was successful only for targets directly ahead of the model bat.

Animals↗

The bat head-related transfer function reveals binaural cues for sound localization in azimuth and elevation.

Directional properties of the sound transformation at the ear of four intact echolocating bats, Eptesicus fuscus, were investigated via measurements of the head-related transfer function (HRTF). Contributions of external ear structures to directional features of the transfer functions were examined by remeasuring the HRTF in the absence of the pinna and tragus. The investigation mainly focused on the interactions between the spatial and the spectral features in the bat HRTF. The pinna provides gain and shapes these features over a large frequency band (20-90 kHz), and the tragus contributes gain and directionality at the high frequencies (60 to 90 kHz). Analysis of the spatial and spectral characteristics of the bat HRTF reveals that both interaural level differences (ILD) and monaural spectral features are subject to changes in sound source azimuth and elevation. Consequently, localization cues for horizontal and vertical components of the sound source location interact. Availability of multiple cues about sound source azimuth and elevation should enhance information to support reliable sound localization. These findings stress the importance of the acoustic information received at the two ears for sound localization of sonar target position in both azimuth and elevation.

Animals↗

The sound emission pattern and the acoustical role of the noseleaf in the echolocating bat, Carollia perspicillata.

Carollia perspicillata (Phyllostomidae) is a frugivorous bat that emits low-intensity, broadband, frequency-modulated echolocation pulses through nostrils surrounded by a noseleaf. The emission pattern of this bat is of interest because the ratio between the nostril spacing and the emitted wavelength varies during the pulse, causing complex interference patterns in the horizontal dimension. Sound pressures around the bat were measured using a movable microphone and were referenced to those at a stationary microphone positioned directly in front of the animal. Interference between the nostrils was confirmed by blocking one nostril, which eliminated sidelobes and minima in the emission pattern, and by comparison of real emission patterns with simple computer models. The positions of minima in the patterns indicate effective nostril spacings of over a half-wavelength. Displacement of the dorsal lancet of the noseleaf demonstrated that this structure directs sound in the vertical dimension.

Acoustics↗

Clutter interference and the integration time of echoes in the echolocating bat, Eptesicus fuscus.

The ability of the echolocating bat, Eptesicus fuscus, to detect a sonar target is affected by the presence of other targets along the same axis at slightly different ranges. If echoes from one target arrive at about the same delay as echoes from another target, clutter interference occurs and one set of echoes masks the other. Although the bat's sonar emissions and the echoes themselves are 2 to 5 ms long, echoes (of approximately equal sensation levels--around 15 dB SL) only interfere with each other if they arrive within 200 to 400 microseconds of the same arrival time. This figure is an estimate of the integration time of the bat's sonar receiver for echoes. The fine structure of the clutter-interference data reflects the reinforcement and cancellation of echoes according to their time separation. When clutter interference first occurs, the waveforms of test and cluttering echoes already overlap for much of their duration. The masking effect underlying clutter interference appears specifically due to overlap, not between raw echo waveforms, but between the patterns of mechanical excitation created when echoes pass through bandpass filters equivalent to auditory-nerve tuning curves. While the time scale of clutter interference is substantially shorter than the duration of echo waveforms, it still is much longer than the eventual width of a target's range-axis image expressed in terms of echo delay.

Animals↗