Biosonar resolving power: echo-acoustic perception of surface structures in the submillimeter range.

The minimum distance for which two points still can be separated from each other defines the resolving power of a visual system. In an echo-acoustic context, the resolving power is usually measured as the smallest perceivable distance of two reflecting surfaces on the range axis and is found to be around half a millimeter for bats employing frequency modulated (FM) echolocation calls. Only few studies measured such thresholds with physical objects, most often bats were trained on virtual echoes i.e., echoes generated and played back by a computer; moreover, bats were sitting while they received the stimuli. In these studies differences in structure depth between 200 and 340 µm were found. However, these low thresholds were never verified for free-flying bats and real physical objects. Here, we show behavioral evidence that the echo-acoustic resolving power for surface structures in fact can be as low as measured for computer generated echoes and even lower, sometimes below 100 µm. We found this exceptional fine discrimination ability only when one of the targets showed spectral interferences in the frequency range of the bats' echolocation call while the other target did not. This result indicates that surface structure is likely to be perceived as a spectral quality rather than being perceived strictly in the time domain. Further, it points out that sonar resolving power directly depends on the highest frequency/shortest wavelength of the signal employed.

Floral acoustics: conspicuous echoes of a dish-shaped leaf attract bat pollinators.

The visual splendor of many diurnal flowers serves to attract visually guided pollinators such as bees and birds, but it remains to be seen whether bat-pollinated flowers have evolved analogous echo-acoustic signals to lure their echolocating pollinators. Here, we demonstrate how an unusual dish-shaped leaf displayed above the inflorescences of the vine Marcgravia evenia attracts bat pollinators. Specifically, this leaf's echoes fulfilled requirements for an effective beacon, that is, they were strong, multidirectional, and had a recognizable invariant echo signature. In behavioral experiments, presence of the leaves halved foraging time for flower-visiting bats.

Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia).

BACKGROUND: Bats of the family Phyllostomidae show a unique diversity in feeding specializations. This taxon includes species that are highly specialized on insects, blood, small vertebrates, fruits or nectar, and pollen. Feeding specialization is accompanied by morphological, physiological and behavioural adaptations. Several attempts were made to resolve the phylogenetic relationships within this family in order to reconstruct the evolutionary transitions accompanied by nutritional specialization. Nevertheless, the evolution of nectarivory remained equivocal. RESULTS: Phylogenetic reconstructions, based on a concatenated nuclear-and mitochondrial data set, revealed a paraphyletic relationship of nectarivorous phyllostomid bats. Our phylogenetic reconstructions indicate that the nectarivorous genera Lonchophylla and Lionycteris are closer related to mainly frugivorous phyllostomids of the subfamilies Rhinophyllinae, Stenodermatinae, Carolliinae, and the insectivorous Glyphonycterinae rather than to nectarivorous bats of the Glossophaginae. This suggests an independent origin of morphological adaptations to a nectarivorous lifestyle within Lonchophyllinae and Glossophaginae. Molecular clock analysis revealed a relatively short time frame of about ten million years for the divergence of subfamilies. CONCLUSIONS: Our study provides strong support for diphyly of nectarivorous phyllostomids. This is remarkable, since their morphological adaptations to nutrition, like elongated rostrums and tongues, reduced teeth and the ability to use hovering flight while ingestion, closely resemble each other. However, more precise examinations of their tongues (e.g. type and structure of papillae and muscular innervation) revealed levels of difference in line with an independent evolution of nectarivory in these bats.

Complex vocal imitation during ontogeny in a bat.

Vocal imitation--the ability to learn a previously unknown acoustic signal from a tutor--is considered to be a key innovation in the evolution of speech. This faculty is very rare and patchily distributed within the animal kingdom, suggesting multiple instances of convergent evolution. It has long been predicted that bats should be capable of vocal imitation and our results provide evidence for this phenomenon. We report that pups of the bat Saccopteryx bilineata learn a complex vocalization through vocal imitation. During ontogeny, pups of both sexes imitate territorial song from adult males, starting with simple precursor songs that develop into genuine renditions. The resemblance of pup renditions to their acoustic model is not caused by physical maturation effects, is independent of pups' gender and relatedness towards adult males and becomes more pronounced during ontogeny, showing that auditory experience is essential for vocal development. Our findings indicate that the faculty of vocal imitation is more widespread than previously thought and emphasize the importance of research on audiovocal communication in bats for a better understanding of the evolutionary origin of vocal imitation.

Effects of artificial roosts for frugivorous bats on seed dispersal in a neotropical forest pasture mosaic.

In the Neotropics ongoing deforestation is producing open and heavily fragmented landscapes dominated by agriculture, mostly plantations and cattle pastures. After some time agriculture often becomes uneconomical and land is abandoned. Subsequent habitat regeneration may be slow because seed inputs are restricted by a lack of incentives--such as suitable roost sites--for seed dispersers to enter deforested areas. Increasing environmental awareness has fostered growing efforts to promote reforestation. Practical and cost-efficient methods for kick-starting forest regeneration are, however, lacking. We investigated whether artificial bat roosts for frugivorous bat species can attract these key seed dispersers to deforested areas, thereby increasing seed rain. We installed artificial bat roosts in a forest-pasture mosaic in the Costa Rican Atlantic lowlands and monitored bat colonization and seed dispersal. Colonization occurred within a few weeks of installation, and 10 species of bats occupied the artificial roosts. Five species of frugivorous or nectarivorous bats colonized artificial roosts permanently in both primary habitat and in deforested areas, in numbers similar to those found in natural roosts. Seed input around artificial roosts increased significantly. Sixty-nine different seed types, mostly of early-successional plant species, were transported by bats to artificial roosts in disturbed habitats. The installation of artificial bat roosts thus successfully attracted frugivorous bats and increased seed inputs into degraded sites. This method is likely to speed up early-vegetation succession, which in turn will attract additional seed dispersers, such as birds, and provide a microhabitat for seeds of mid- and late-successional plants. As well as supporting natural forest regeneration and bat conservation, this cost-efficient method can also increase environmental awareness among landowners.

How to budget metabolic energy: torpor in a small Neotropical mammal.

Neotropical nectar-feeding bats (Glossophaginae) are highly specialized in the exploitation of floral nectar and have one of the highest mass-specific metabolic rates among mammals. Nevertheless, they are distributed throughout the tropics and subtropics over a wide elevational range, and thus encounter many extreme and energetically challenging environmental conditions. Depressing their otherwise high metabolic rate, e.g., in situations of food restriction, might be an important adaptive physiological strategy in these dietary specialists. We investigated the thermoregulatory behavior of captive 10-g nectar feeding bats (Glossophaga soricina; Chiroptera, Phyllostomidae) under variable ambient temperatures (T (a)) and feeding regimes and predicted that bats would use torpor as an energy-conserving behavior under energetic constraints. All tested animals entered torpor in response to energetic restrictions and the depth of torpor was dependent on the body condition of the animals and hence on their degree of physiological constraints. Periods of torpor with body temperatures (T (b)) below 34 degrees C were precisely adjusted to the photoperiod. The median length of diurnal torpor was 11.43 h. The lowest T (b) measured was 21 degrees C at a T (a) of 19 degrees C. Estimated energy savings due to torpor were considerable, with reductions in metabolic rate to as low as 5% of the metabolic rate of normothermic bats at the same T (a). However, contrary to temperate zone bats that also employ diurnal torpor, G. soricina regulated their T (b) to the highest possible levels given the present energetic supplies. To summarize, G. soricina is a precise thermoregulator, which strategically employs thermoregulatory behavior in order to decrease its energy expenditure when under energetic restrictions. This adaptation may play a crucial role in the distribution and the assembly of communities of nectar-feeding bats and may point to a general capacity for torpor in tropical bats.

Size discrimination of hollow hemispheres by echolocation in a nectar feeding bat.

Nectar feeding bats use echolocation to find their flowers in the dense growth of tropical rainforests, and such flowers have evolved acoustic features that make their echo more conspicuous to their pollinators. To shed light on the sensory and cognitive basis of echoacoustic object recognition we conducted a size discrimination experiment with the nectarivorous bat Glossophaga soricina and compared the bats' behavioural performance with the echoic features of the training objects. We chose a simple geometric form, the hollow hemisphere, as the training object because of its resemblance to the bell-shaped concave form of many bat flowers, as well as its special acoustic qualities. The hemispheres showed a characteristic echo pattern, which was constant over a wide range of angles of sound incidence. We found systematic size-dependent changes in the echo's temporal and spectral pattern as well as in amplitude. Bats were simultaneously confronted with seven different sizes of hollow hemispheres presented from their concave sides. Visits to one particular size were rewarded with sugar water, while we recorded the frequency of visits to the unrewarded hemispheres. We found that: (1) bats learned to discriminate between hemispheres of different size with ease; (2) the minimum size difference for discrimination was a constant percentage of the hemisphere's size (Weber fraction: approximately 16% of the radius); (3) the comparison of behavioural data and impulse response measurements of the objects' echoes yielded discrimination thresholds for mean intensity differences (1.3 dB), the temporal pattern (3-22 micros) and the change of spectral notch frequency (approximately 16%). We discuss the advantages of discrimination in the frequency and/or time domain.

'Binaural echo disparity' as a potential indicator of object orientation and cue for object recognition in echolocating nectar-feeding bats.

Echolocating bats emit ultrasonic calls through their mouth or their nostrils and receive echoes from objects with both their ears. Information conveyed in the echoes is the basis for their three-dimensional acoustic perception of the surroundings. The direction of an object is encoded in binaural echo differences, i.e. on the one hand in the different arrival times of its echo at the two ears, and on the other hand in spectral differences through direction-dependent frequency filtering of head and pinnae. Insufficient attention has been paid, however, to the fact that three-dimensional objects produce structured spatial echo fields, and that the position of the ear in this field determines the echo it receives. We were interested to determine whether the two ears, in addition to direction-specific echo differences, receive object-specific echo disparities that might be useful for the bat. Our measurements with an artificial bat head, which consisted of two microphones and a small ultrasound loudspeaker arranged to resemble a bat's ears and mouth, revealed that echoes at the two ears differed largely depending on the shape and orientation of the echo-giving object. Binaural echo disparities of a bat-pollinated flower did indeed carry information about the orientation and, to a lesser extent, the shape of the flower. During flower approach such object-specific binaural echo disparities even exceed the binaural differences encoding direction of echo incidence, because the echo from the flower in front undergoes the same directional filtering by the two symmetrical ears. Nectar-feeding bats could use these object-specific binaural echo disparities not only to determine the object's orientation relative to the approaching bat, facilitating flight planning, but also to improve object recognition through spatial reconstruction of details of the object creating the echo. Our results suggest that the evaluation of binaural echo disparity has a greater importance for these tasks than has previously been assumed.

Babbling behavior in the sac-winged bat (Saccopteryx bilineata).

Infant babbling in humans and a few other primates plays an important role in allowing the young to practice the adult vocal repertoire during early behavioral development. Vocalizations uttered during babbling resemble, to some degree, the acoustic structure of adult vocalizations and are often produced in long bouts independent of any social context. Similar behavior, termed subsong or plastic song, is known from a variety of songbirds. Here, we show that pups of the sac-winged bat (Saccopteryx bilineata), a species with an unusually large vocal repertoire, produce renditions of all known adult vocalization types during bouts of vocalizations, which appear to be independent of a distinct social context. Babbling occurs in pups of both sexes, even though only adult males, not females, utter all different vocalization types produced in infancy. To our knowledge, this is the first evidence of babbling in a nonprimate mammal and suggests that infant babbling may be necessary for the ontogeny of complex vocal repertoires.

Flight and echolocation behaviour of whiskered bats commuting along a hedgerow: range-dependent sonar signal design, Doppler tolerance and evidence for 'acoustic focussing'.

Echolocating bats obtain three-dimensional images of their surroundings in complete darkness by emitting sonar signals and evaluating returning echoes. When flying close to objects, bats risk collision and therefore depend on the accuracy of images--particularly in the perceived distance of obstacles, which is coded by the time delay between call and echo. Yet, during flight, such accuracy is perturbed first because bats call and receive echoes at different positions and second because echoes are modified by Doppler shifts. Certain call designs avoid both sources of ranging error, but only for a limited range of distances [the 'distance of focus' (DOF)]. Here, we show that whiskered bats (Myotis mystacinus) using broadband echolocation calls adjust call design in a range-dependent manner so that nearby obstacles are localised accurately. Such behaviour is adaptive because it reduces collision risk. The bats also reduced call duration to some extent as they approached obstacles so that most returning echoes arrived after they finished calling. This reduction in call duration during the approach to obstacles was neither the only nor the main factor that influenced DOF. Indeed, both duration and bandwidth of calls influenced DOF independently, with lower bandwidths and longer durations giving greater DOF. Our findings give a new perspective on the adaptive significance of echolocation call design in nature and have implications for sonar engineering.

Blood-sucking bugs as a gentle method for blood-collection in water budget studies using doubly labelled water.

During doubly-labelled water (DLW) experiments, blood collection by venous puncture may traumatize animals and consequently affect the animals' behaviour and energy budget. Recent studies have shown that blood-sucking bugs (Triatominae; Heteroptera) can be used instead of conventional needles to obtain blood from animals. In this paper, we validate the bug method in captive nectar-feeding bats, Glossophaga soricina, for water budget analysis by comparing the daily water flux estimated with the DLW method with values measured by an energy balance method. As the mean daily water flux of the DLW method was not significantly deviating from the expected value, blood-sucking bugs may substitute more invasive methods of blood collection in DLW experiments. Based on the DLW estimates, daily energy and water intake rates were calculated and compared to values measured with the energy balance method. The DLW method and the energy balance method yielded on average similar results regarding the daily energy intake (DLW method: 48.8+/-14.2 kJ d(-1) versus energy balance method: 48.1+/-9.9 kJ d(-1)) and daily water intake (DLW method: 13.7+/-2.4 mL d(-1) versus energy balance method: 14.7+/-3.0 mL d(-1)). Based on the calculated water and sugar intake per day, we estimated the sugar concentration of ingested nectar to equal on average 16.2+/-2.4% (mass/mass), which fell close to the measured sugar concentration of 17% (mass/mass) bats fed on during the experiment. We conclude that it is possible to extrapolate mean daily energy and water intake for animal groups, populations and species based on DLW estimates, but due to the large variance of results (low accuracy), it seems inadequate to calculate values for single individuals.

Ultraviolet vision in a bat.

Most mammals, with the exception of primates, have dichromatic vision and correspondingly limited colour perception. Ultraviolet vision was discovered in mammals only a decade ago, and in the few rodents and marsupials where it has been found, ultraviolet light is detected by an independent photoreceptor. Bats orient primarily by echolocation, but they also use vision. Here we show that a phyllostomid flower bat, Glossophaga soricina, is colour-blind but sensitive to ultraviolet light down to a wavelength of 310 nm. Behavioural experiments revealed a spectral-sensitivity function with maxima at 510 nm (green) and above 365 nm (ultraviolet). A test for colour vision was negative. Chromatic adaptation had the same threshold-elevating effects on ultraviolet and visible test lights, indicating that the same photoreceptor is responsible for both response peaks (ultraviolet and green). Thus, excitation of the beta-band of the visual pigment is the most likely cause of ultraviolet sensitivity. This is a mechanism for ultraviolet vision that has not previously been demonstrated in intact mammalian visual systems.

Genetic mating system and the significance of harem associations in the bat Saccopteryx bilineata.

We analysed the polygynous mating system of the bat Saccopteryx bilineata using behaviour observations and genetic data on 11 microsatellite DNA loci. Basic social units in S. bilineata are harem groups that consist of single males and up to eight females. Colonies comprise several harem groups, and the composition of colonies and harems is often stable over several reproductive seasons. The combination of parentage exclusion and likelihood-based parentage assignment in this study produced detailed parentage information for a large colony of S. bilineata. Reproduction occurred mostly within the colony (17% extra-colony paternity), but social associations in harems within the colony did not represent reproductive units (70% extra-harem paternity). The latter finding was consistent over three reproductive seasons. Spatial association of the roosting sites of males and females could not explain parentage patterns in the colony. Even though intra-harem paternity was less frequent than expected, it contributed significantly to reproduction of harem males. On average, the number of offspring sired by a male with females in his harem territory increased significantly with harem size, which corresponds to the higher energetic investment that is related to the maintenance of large harems. However, extra-harem paternity was not correlated with a male's harem size or intra-harem reproductive success. This suggests that individual preferences of females rather than male traits associated with the ability to defend large harems are most likely to cause the detected differences between social association and genetic mating system.