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Auditory sensitivity and frequency selectivity in greater spear-nosed bats suggest specializations for acoustic communication.

We investigated the relationship between auditory sensitivity, frequency selectivity, and the vocal repertoire of greater spear-nosed bats ( Phyllostomus hastatus). P. hastatus commonly emit three types of vocalizations: group-specific foraging calls that range from 6 to 11 kHz, low amplitude echolocation calls that sweep from 80 to 40 kHz, and infant isolation calls from 15 to 100 kHz. To determine if hearing in P. hastatus is differentially sensitive or selective to frequencies in these calls, we determined absolute thresholds and masked thresholds using an operant conditioning procedure. Both absolute and masked thresholds were lowest at 15 kHz, which corresponds with the peak energy of isolation calls. Auditory and masked thresholds were higher at sound frequencies used for group-specific foraging calls and echolocation calls. Isolation calls meet the requirements of individual signatures and facilitate parent-offspring recognition. Many bat species produce isolation calls with peak energy between 10 and 25 kHz, which corresponds with the frequency region of highest sensitivity in those species for which audiogram data are available. These findings suggest that selection for accurate offspring recognition exerts a strong influence on the sensory system of P. hastatus and likely on other species of group-living bats.

Acoustic Stimulation↗

Vocal communication in adult greater horseshoe bats, Rhinolophus ferrumequinum.

Whereas echolocation in horseshoe bats is well studied, virtually nothing is known about characteristics and function of their communication calls. Therefore, the communication calls produced by a group of captive adult greater horseshoe bats were recorded during various social interactions in a free-flight facility. Analysis revealed that this species exhibited an amazingly rich repertoire of vocalizations varying in numerous spectro-temporal aspects. Calls were classified into 17 syllable types (ten simple syllables and seven composites). Syllables were combined into six types of simple phrases and four combination phrases. The majority of syllables had durations of more than 100 ms with multiple harmonics and fundamental frequencies usually above 20 kHz, although some of them were also audible to humans. Preliminary behavioral observations indicated that many calls were emitted during direct interaction with and in response to social calls from conspecifics without requiring physical contact. Some echolocation-like vocalizations also appeared to clearly serve a communication role. These results not only shed light upon a so far widely neglected aspect of horseshoe bat vocalizations, but also provide the basis for future studies on the neural control of the production of communicative vocalizations in contrast to the production of echolocation pulse sequences.

Age Factors↗

Psychometric function for nectar volume perception of a flower-visiting bat.

For foraging pollinators one aspect of floral quality is the volume of nectar available. Thus, nectar-feeding animals should be able to estimate volumes of received nectar. In this study, we determined the psychometric function for nectar volume discrimination of a Neotropical flower-visiting bat Glossophaga soricina. For this, we examined the ability of bats to discriminate between two nectar volumes in a two-alternative forced-choice paradigm. We used a Bayesian inference approach to determine psychometric functions. From the derived psychometric function we assessed the discrimination threshold at a value of 0.69. G. soricina could clearly distinguish between two volumes, when the difference between the two nectar volumes divided by their average exceeded this value. This indicates that bats possess a sense for the perception and discrimination of volumes of nectar that is better developed than in honeybees.

Animals↗

Discrimination of sinusoidally frequency-modulated sound signals mimicking species-specific communication calls in the FM-bat Phyllostomus discolor.

In the lesser spear-nosed bat, Phyllostomus discolor, maternal directive calls are characterized by an individual type of sinusoidal frequency modulation (= SFM) pattern. Beside modulation frequency, modulation depth, carrier frequency, and number of modulation cycles per call contribute to the mother's vocal signature. Since juvenile P. discolor learn to adapt their isolation calls to the corresponding call characteristics of the own mother or even to playback of a computer-stored directive call, if hand-reared in the absence of conspecifics, the bats' auditory system ought to be able to resolve interindividual differences in communication call structure. However, quantitative psychoacoustic data on the discrimination of SFM signals in this species are not available. Thus, in the present study, lesser spear-nosed bats were trained in a two-alternative forced-choice procedure to discriminate between two alternatingly presented SFM sound signals differing in modulation frequency. Other characteristics of acoustic stimuli were identical and designed to mimick the fundamental of species-specific calls. By gradually reducing the difference in modulation frequency between both stimuli within the behavioural relevant range until the animals' performance dropped below the 75%-correct level, a considerable auditory spectro-temporal resolution has been revealed. Particularly in comparison to the overall interindividual variation of this call parameter (minimal modulation frequency = 49 Hz, maximum = 100 Hz), the determined average difference limen for modulation frequency of 2.42 +/- 0.29 Hz seems substantial and sufficient for labelling individuals.

Acoustic Stimulation↗

Frequency tuning, latencies, and responses to frequency-modulated sweeps in the inferior colliculus of the echolocating bat, Eptesicus fuscus.

Neurons in the inferior colliculus (IC) of the awake big brown bat, Eptesicus fuscus, were examined for joint frequency and latency response properties which could register the timing of the bat's frequency-modulated (FM) biosonar echoes. Best frequencies (BFs) range from 10 kHz to 100 kHz with 50% tuning widths mostly from 1 kHz to 8 kHz. Neurons respond with one discharge per 2-ms tone burst or FM stimulus at a characteristic latency in the range of 3-45 ms, with latency variability (SD) of 50 microseconds to 4-6 ms or more. BF distribution is related to biosonar signal structure. As observed previously, on a linear frequency scale BFs appear biased to lower frequencies, with 20-40 kHz overrepresented. However, on a hyperbolic frequency (linear period) scale BFs appear more uniformly distributed, with little overrepresentation. The cumulative proportion of BFs in FM1 and FM2 bands reconstructs a scaled version of the spectrogram of FM broadcasts. Correcting FM latencies for absolute BF latencies and BF time-in-sweep reveals a subset of IC cells which respond dynamically to the timing of their BFs in FM sweeps. Behaviorally, Eptesicus perceives echo delay and phase with microsecond or even submicrosecond accuracy and resolution, but even with use of phase-locked FM and tone-burst stimuli the cell-by-cell precision of IC time-frequency registration seems inadequate by itself to account for the temporal acuity exhibited by the bat.

Animals↗

Binaural influences on Doppler shift compensation of the horseshoe bat Rhinolophus rouxi.

The flying horseshoe bat Rhinolophus rouxi compensates for Doppler shifts in echoes of their orientation pulses. By lowering the frequency of subsequent calls the echo's constant frequency is stabilized at the so-called reference frequency centered in a narrow and sensitive cochlear filter. This audio-vocal behaviour is known as Doppler shift compensation. To investigate whether the bats depend on binaural cues when compensating, three animals were tested for compensation on a swing before and after unilateral deafening. In each case compensation was severely impaired by unilateral deafening. Individual animals' compensation amplitude was reduced to 28-48% of the preoperational compensation of a +1.8 kHz shift. Doppler shift compensation performance did not recover to control levels during the observed period of 24 h after surgery. In contrast, unilateral middle ear removal which induces a unilateral auditory threshold increase of 9-14 dB does not impair compensation performance on the swing. To mimick Doppler shifts in a fixed setup, the frequencies of recorded echolocation calls were experimentally shifted between 0 and +2 kHz and played back via earphones to six animals. The bats completely compensated the experimental shifts only as long as the interaural intensity difference of the playback did not exceed 20 dB. No animal compensated with monaural playback.

Adaptation, Physiological↗

Field metabolic rates of phytophagous bats: do pollination strategies of plants make life of nectar-feeders spin faster?

Recently, it was argued that extrinsic factors, such as high foraging costs, lead to elevated field metabolic rates (FMR). We tested this suggestion by comparing the FMR of nectar-feeding and fruit-eating bats. We hypothesized that the foraging effort per energy reward is higher for nectar-feeding mammals than for fruit-eating mammals, since energy rewards at flowering plants are smaller than those at fruiting plants. Using the doubly labelled water method, we measured the FMR of nectar-feeding Glossophaga commissarisi and fruit-eating Carollia brevicauda, which coexisted in the same rainforest habitat and shared the same daytime roosts. Mass-specific FMR of G. commissarisi exceeded that of C. brevicauda by a factor of almost two: 5.3+/-0.6 kJ g(-1) day(-1) for G. commissarisi and 2.8+/-0.4 kJ g(-1) day(-1) for C. brevicauda. Since nectar-feeding bats imbibe nectar droplets of only 193 J energy content during each flower visit, a G. commissarisi bat has to perform several 100 flower visits per night to meet its energy requirement. The fruit-eating C. brevicauda, on the other hand, needs to harvest only 3-12 Piper infructescenses per night, as the energy reward per Piper equals ca. 6-30 kJ. We argue that the flowering and fruiting plants exert different selective forces on the foraging behaviour and energetics of pollinators and the seed dispersers, respectively. A comparison between nectar-feeding and non-nectar-feeding species in various vertebrate taxa demonstrates that pollinators have elevated FMRs.

Animals↗

Plasma leptin decreases during lactation in insectivorous bats.

We previously demonstrated high leptin levels during late pregnancy in little brown bats (Myotis lucifugus). We now extend these observations to a second species, the big brown bat (Eptesicus fuscus), and also report that leptin increases after the first trimester of pregnancy. Leptin decreased to baseline 1 week following parturition, with a half-time decay of 2 days. During lactation, leptin was significantly correlated with body mass in E. fuscus, but not in M. lucifugus. No circadian pattern of leptin was observed in M. lucifugus. The decrease in post-partum leptin in bats may be partly explained by loss of putative placental leptin. The continued decrease may reflect depletion of body fat during this energy demanding period, at least in Eptesicus. Changes in leptin during lactation appeared to be independent of circadian effects and time of sampling. Our study provides additional evidence that leptin increases during pregnancy and declines during lactation in a free-ranging mammal, supporting the hypothesis that leptin plays important but yet undetermined roles in reproduction.

Animals↗

Diurnal and seasonal changes in blood composition of the free-living Egyptian fruit bat (Rousettus aegyptiacus).

We studied the blood profile of the free-living fruit bat (Rousettus aegyptiacus) during the beginning of the activity period (around various feeding trees) and upon return to the day roost during 1994-1995. Results of the present study suggest that during winter and early spring bats are characterized by a poor physical and physiological state as reflected in the blood profile, revealing elevated urea and uric acid concentrations. It was found that at the end of the resting phase, R. aegyptiacus was in a mild state of dehydration (increased hematocrit and hemoglobin levels). At the end of activity, upon return to the day roost, both hematocrit and hemoglobin levels decreased but bats still maintained a high plasma osmolality. Several components in the blood are effected by the feeding time and show a cyclic change in concentration. The reverse relationship between glucose and triglyceride levels may indicate that glucose is the energy source during the active phase and that fat is the energy source during the resting period. The low cholesterol level in the blood reflects its absence in the fruit diet.

Animals↗

Neural ensemble coding of target identity in echolocating bats.

Most insectivorous bats use echolocation to determine the identity of flying insects. Among the many target features that are so extracted, the insect's wingbeat pattern and frequency appear to serve as useful cues for identification. Biosonar pulses impinging on the fluttering wings of an insect are returned as echoes whose amplitudes vary with time, thus providing a characteristic signature of the insect. It has been shown previously that neurons in the inferior colliculus, a midbrain auditory nucleus, of the little brown bat respond to sound stimuli that mimic echoes from fluttering targets. To examine the manner in which target identity is represented in the inferior colliculus, an ensemble coding analysis using a filter-based approach was undertaken. The analysis indicates that a discrete subset of neurons in the inferior colliculus, the onset units, are strongly tuned to wingbeat frequencies of targets that the bat hunts, and that ensemble response reaches a maximum at a distinct phase of the prey capture maneuver: the late approach stage. On the basis of the analysis it is hypothesized that inferior colliculus neurons may play an important role in target detection-identification processing. Although ensemble coding of temporally sequenced information has not been analyzed in the auditory system so far, this study indicates that this method of coding may provide the information necessary to detect and identify targets during prey capture.

Acoustic Stimulation↗

Cytoarchitecture of the medial geniculate body and thalamic projections to the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi). I. Temporal fields.

The auditory cortex in echolocating bats is one of the best studied in mammals, yet the projections of the thalamus to the different auditory cortical fields have not been systematically analyzed in any bat species. The data of the present study were collected as part of a combined investigation of physiological properties, neuroarchitecture, and chemoarchitecture as well as connectivity of cortical fields in Rhinolophus in order to establish a neuroanatomically and functionally coherent view of the auditory cortex in the horseshoe bat. This paper first describes the neuroanatomic parcellation of the medial geniculate body and then concentrates on the afferent thalamic connections with auditory cortical fields of the temporal region. Deposits of horseradish peroxidase and wheatgerm-agglutinated horseradish peroxidase were made into neurophysiologically characterized locations of temporal auditory cortical fields; i.e., the tonotopically organized primary auditory cortex, a ventral field, and a temporal subdivision of a posterior dorsal field. A clear topographic relationship between thalamic subdivisions and specific cortical areas is demonstrated. The primary auditory cortex receives topographically organized input from the central ventral medial geniculate body. The projection patterns to the temporal subdivision of the posterior dorsal field suggest that it is a "core" field, similar to the posterior fields in the cat. Projections to the ventral field arise primarily from border regions of the ventral medial geniculate body. On the whole, the organization of the medial geniculate body projections to the temporal auditory cortex is quite similar to that described in other mammals, including cat and monkey.

Animals↗

Thalamic projections to the auditory cortex in the rufous horseshoe bat (Rhinolophus rouxi). II. Dorsal fields.

In this study, we analyzed the thalamic connections to the parietal or dorsal auditory cortical fields of the horseshoe bat, Rhinolophus rouxi. The data of the present study were collected as part of a combined investigation of physiologic properties, neuroarchitecture, and chemoarchitecture as well as connectivity of cortical fields in Rhinolophus, in order to establish a neuroanatomically and functionally coherent view of the auditory cortex. Horseradish peroxidase or wheat-germ-agglutinated horseradish peroxidase deposits were made into cortical fields after mapping response properties. The dorsal fields of the auditory cortex span nearly the entire parietal region and comprise more than half of the non-primary auditory cortex. In contrast to the temporal fields of the auditory cortex, which receive input mainly from the ventral medial geniculate body (or "main sensory nucleus"), the dorsal fields of the auditory cortex receive strong input from the "associated nuclei" of the medial geniculate body, especially from the anterior dorsal nucleus of the medial geniculate body. The anterior dorsal nucleus is as significant for the dorsal fields of the auditory cortex as the ventral nucleus of the medial geniculate body is for the temporal fields of the auditory cortex. Additionally, the multisensory nuclei of the medial geniculate body provide a large share of the total input to the nonprimary fields of the auditory cortex. Comparing the organization of thalamic auditory cortical afferents in Rhinolophus with other species demonstrates the strong organizational similarity of this bat's auditory cortex with that of other mammals, including primates, and provides further evidence that the bat is a relevant and valuable model for studying mammalian auditory function.

Animals↗

Exploring the boundary between pollination syndromes: bats and hummingbirds as pollinators of Burmeistera cyclostigmata and B. tenuiflora (Campanulaceae).

In this study I documented the degree of specialization in the pollination systems of Burmeistera cyclostigmata and B. tenuiflora (Campanulaceae) to explore the potential role of floral isolation in the diversification of the genus. I asked which floral characteristics are important in specializing on either bat or hummingbird pollination, and whether overlap between these floral syndromes can exist. I examined nocturnal and diurnal pollen deposition, pollinator visitation rates, and single visit effectiveness and related them to intra- and interspecific variation in Burmeistera floral characteristics at Monteverde, Costa Rica. Bats and hummingbirds visited both Burmeistera species, and bats pollinated both species. Owing to differences in floral morphology, however, hummingbirds effectively pollinated only B. tenuiflora. The generalized pollination system of B. tenuiflora demonstrates that there can be overlap in the boundary between ornithophily and chiropterophily, and that nectar production and timing of anthesis do not serve as barriers between these syndromes. The high intraspecific variation in floral color from green to red or purple did not correlate with either nocturnal or diurnal pollen deposition. Degree of flower accessibility did affect pollination; nocturnal pollen deposition significantly decreased as flowers become more obstructed. In Burmeistera, floral morphology and accessibility appear to be the most important floral characteristics for specialization at the boundary between ornithophily and chiropterophily.

Animals↗

On the density-dependence of seed predation in Dipteryx micrantha, a bat-dispersed rain forest tree.

We studied the effect of seed density on seed predation by following the fate of bat-dispersed Dipteryx micrantha (Leguminosae) seeds deposited under bat feeding roosts. The study was conducted in Cocha Cashu biological station, Amazonian Peru, during the fruiting period of Dipteryx. Predation of Dipteryx seeds in the area is mainly by large to medium-sized rodents. Seed deposits beneath bat feeding roosts were monitored for a 13-week period in an 18-ha study area. A total of 210 seed deposits were found, and on average, seed predators encountered 22% of them during any one week. About one-third of the seed deposits escaped predation, and those deposits that had relatively few seeds were more likely to go unnoticed by rodents than were deposits with many seeds. The mean seed destruction rate was 8% per week; deposits with many seeds tended to lose a smaller proportion of their seeds to seed predators than did deposits with few seeds. Regression tests for the weekly data showed that, at the beginning of the observation period, seed predation was not density-dependent. Later, when the total seed crop beneath roosts was high, the number of seeds predated per deposit was positively density-dependent, while the proportion of seeds predated was negatively density-dependent, indicating predator satiation. Seed deposits that had been visited by seed predators once had a higher probability of being revisited the week after, especially if they contained many seeds when first encountered. This indicates that the foraging behavior of rodents may be affected by their remembering the location of seed-rich patches.

Animals↗

Consequences of outer hair cell damage for otoacoustic emissions and audio-vocal feedback in the mustached bat.

The cochlea of the mustached bat is adapted to process ultrasonic echolocation signals. To assess the involvement of active sound amplification by outer hair cells in high-frequency hearing and in audio-vocal interaction, selective hair cell damage was induced by the antibiotic Amikacin. Amikacin preferentially damaged the first row of outer hair cells in the basal cochlear turn. The cochlear regions coding for the second-harmonic constant-frequency component of the echolocation call (CF2) at 61 kHz and for frequencies between 75 and 100 kHz were the most affected. This was reflected in an increase of mechanical thresholds obtained by measuring distortion-product otoacoustic emissions. During initial periods of minor hair cell damage, when thresholds had deteriorated by less than 40 dB, a sharp, mechanical, cochlear resonance that is responsible for enhanced tuning to 61 kHz was still measurable as a stimulus-frequency otoacoustic emission and its frequency decreased by 350 Hz. The persistence of the resonance suggests that passive structures like the tectorial or basilar membrane are important for generation of the resonance. Behaviorally, the bats reacted to the change in cochlear micromechanics with a decrease of their CF2 frequency by 360 Hz. After larger hair cell damage, when the cochlear resonance had disappeared, the bats vocalized only sparsely and the CF2 frequency increased by up to 2 kHz, which may correspond to a state without audiovocal feedback. This indicates that audio-vocal feedback in the nondamaged animal works to lower the call frequency.

Animals↗

Responses of cerebellar neurons of the CF-FM bat, Pteronotus parnellii to acoustic stimuli.

Single units (125) which faithfully discharged action potentials to acoustic stimuli (35 ms in duration with 0.5 ms rise and decay times) were recorded in the cerebellar vermis and hemispheres of the CF-FM bat, Pteronotus parnellii. These units had response latencies between 1.5 and 27 ms and minimum thresholds between 2 and 83.5 dB SPL. Best frequencies (BFs) of these units ranged from 30.32 to 79.28 kHz, but more than half (64 units, 51.2%) were between 59.73 and 63.32 kHz. While most tuning curves of these units were either broad or irregular, those curves with BFs tuned at around 61 kHz which is the frequency of the predominant CF component of the bat's echolocation signals were extremely narrow with Q10-dB values as high as 153. Those units (29) with BFs tuned near the 61 kHz also showed off-responses. These data indicate that auditory specialization for processing of species-specific orientation signals also exists in the cerebellum of this bat.

Animals↗

Mapping of the auditory area in the cerebellar vermis and hemispheres of the mustache bat, Pteronotus parnellii parnellii.

Microelectrode mapping of the auditory areas in the cerebellar vermis and hemispheres of mustache bats, Pteronotus parnellii parnellii, reveals that a large area of the bat's cerebellum contains units responding to acoustic signals. A study of frequency tuning of isolated units shows that there are two large groups of auditory units. The units of one group are sharply tuned to a very narrow band of frequency with BFs between 60 and 64 kHz. The units of the other group are broadly tuned, with BFs between 47 and 59 kHz. These two groups of units are probably involved in processing the predominant CF and FM portions of the bat's orientation sounds during echolocation.

Acoustic Stimulation↗