Dynamics of jamming avoidance in echolocating bats

Animals using active sensing systems such as echolocation or electrolocation may experience interference from the signals of neighbouring conspecifics, which can be offset by a jamming avoidance response (JAR). Here, we report JAR in one echolocating bat (Tadarida teniotis: Molossidae) but not in another (Taphozous perforatus: Emballonuridae) when both flew and foraged with conspecifics. In T. teniotis, JAR consisted of shifts in the dominant frequencies of echolocation calls, enhancing differences among individuals. Larger spectral overlap of signals elicited stronger JAR. Tadarida teniotis showed two types of JAR: (i) for distant conspecifics: a symmetric JAR, with lower- and higher-frequency bats shifting their frequencies downwards and upwards, respectively, on average by the same amount; and (ii) for closer conspecifics: an asymmetric JAR, with only the upper-frequency bat shifting its frequency upwards. In comparison, 'wave-type' weakly electric fishes also shift frequencies of discharges in a JAR, but unlike T. teniotis, the shifts are either symmetric in some species or asymmetric in others. We hypothesize that symmetric JAR in T. teniotis serves to avoid jamming and improve echolocation, whereas asymmetric JAR may aid communication by helping to identify and locate conspecifics, thus minimizing chances of mid-air collisions.     

Object-oriented echo perception and cortical representation in echolocating bats

Echolocating bats can identify three-dimensional objects exclusively through the analysis of acoustic echoes of their ultrasonic emissions. However, objects of the same structure can differ in size, and the auditory system must achieve a size-invariant, normalized object representation for reliable object recognition. This study describes both the behavioral classification and the cortical neural representation of echoes of complex virtual objects that vary in object size. In a phantom-target playback experiment, it is shown that the bat Phyllostomus discolor spontaneously classifies most scaled versions of objects according to trained standards. This psychophysical performance is reflected in the electrophysiological responses of a population of cortical units that showed an object-size invariant response (14/109 units, 13%). These units respond preferentially to echoes from objects in which echo duration (encoding object depth) and echo amplitude (encoding object surface area) co-varies in a meaningful manner. These results indicate that at the level of the bat's auditory cortex, an object-oriented rather than a stimulus-parameter-oriented representation of echoes is achieved.     

Parallel evolution of KCNQ4 in echolocating bats

High-frequency hearing is required for echolocating bats to locate, range and identify objects, yet little is known about its molecular basis. The discovery of a high-frequency hearing-related gene, KCNQ4, provides an opportunity to address this question. Here, we obtain the coding regions of KCNQ4 from 15 species of bats, including echolocating bats that have higher frequency hearing and non-echolocating bats that have the same ability as most other species of mammals. The strongly supported protein-tree resolves a monophyletic group containing all bats with higher frequency hearing and this arrangement conflicts with the phylogeny of bats in which these species are paraphyletic. We identify five parallel evolved sites in echolocating bats belonging to both suborders. The evolutionary trajectories of the parallel sites suggest the independent gain of higher frequency hearing ability in echolocating bats. This study highlights the usefulness of convergent or parallel evolutionary studies for finding phenotype-related genes and contributing to the resolution of evolutionary problems.     

Neural coding of echo-envelope disparities in echolocating bats

The effective use of echolocation requires not only measuring the delay between the emitted call and returning echo to estimate the distance of an ensonified object. To locate an object in azimuth and elevation, the bat’s auditory system must analyze the returning echoes in terms of their binaural properties, i.e., the echoes’ interaural intensity and time differences (IIDs and ITDs). The effectiveness of IIDs for echolocation is undisputed, but when bats ensonify complex objects, the temporal structure of echoes may facilitate the analysis of the echo envelope in terms of envelope ITDs. Using extracellular recordings from the auditory midbrain of the bat, Phyllostomus discolor, we found a population of neurons that are sensitive to envelope ITDs of echoes of their sonar calls. Moreover, the envelope-ITD sensitivity improved with increasing temporal fluctuations in the echo envelopes, a sonar parameter related to the spatial statistics of complex natural reflectors like vegetation. The data show that in bats envelope ITDs may be used not only to locate external, prey-generated rustling sounds but also in the context of echolocation. Specifically, the temporal fluctuations in the echo envelope, which are created when the sonar emission is reflected from a complex natural target, support ITD-mediated echolocation.     

Classification of insects by echolocating greater horseshoe bats

Summary Echolocating greater horseshoe bats (Rhinolophus ferrumequinum) detect insects by concentrating on the characteristic amplitude- and frequency modulation pattern fluttering insects impose on the returning echoes. This study shows that horseshoe bats can also further analyse insect echoes and thus recognize and categorize the kind of insect they are echolocating.Four greater horseshoe bats were trained in a twoalternative forced-choice procedure to choose the echo of one particular insect species turning its side towards the bat (Fig. 1). The bats were able to discriminate with over 90% correct choices between the reward-positive echo and the echoes of other insect species all fluttering with exactly the same wingbeat rate (Fig. 4).When the angular orientation of the reward-positive insect was changed (Fig. 2), the bats still preferred these unknown echoes over echoes from other insect species (Fig. 5) without any further training. Because the untrained bats did not show any prey preference, this indicates that the bats were able to perform an aspect-anglein-dependent classification of insects.Finally we tested what parameters in the echo were responsible for species recognition. It turned out that the bats especially used the small echo-modulations in between glints as a source of information (Fig. 7). Neither the amplitudenor the frequencymodulation of the echoes alone was sufficient for recognition of the insect species (Fig. 8). Bats performed a pattern recognition task based on complex computations of several acoustic parameters, an ability which might be termed cognitive.Abbreviations AM amplitude modulation - CF constant frequency - FM frequency modulation - S+ positive stimulus - S- negative stimulus     

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. Received: 4 December 1995 / Accepted in revised form: 19 April 1996     

Foraging habitats of bats in southern Finland

We determined the foraging habitats of the northern batEptesicus nilssonii (Keyserling et Blasius, 1839), Brandt’s batMyotis brandtii (Eversmann, 1845), whiskered batMyotis mystacinus (Kuhl, 1819), Daubenton’s batMyotis daubentonii (Kuhl, 1819) and brown long-eared batPlecotus auritus (Linnaeus, 1758) in southern Finland. Among these species, we compared the diversities of foraging habitats, linear feature preference and the bats’ tendencies to forage simultaneously.Eptesicus nilssonii was the most opportunistic, foraging in a wide range of habitats.Myotis daubentonii (94%) foraged mainly on water habitats, whileM. brandtii/mystacinus (89%) andP. auritus (66%) foraged mainly in forest habitats. The diversities of foraging habitats used byE. nilssonii andP. auritus were higher than those ofM. brandtii/mystacinus andM. daubentonii. Both E.nilssonii andP. auritus foraged mostly alone or in small numbers, whileM. brandtii/mystacinus tended to gather in large numbers to forage in the same habitat. Half ofE. nilssonii and 46% ofM. daubentonii foraged over linear features, while other species did not use linear features to such an extent. Management and conservation of foraging habitats are needed especially forM. brandtii/mystacinus andM. daubentonii, which are more specialized thanE. nilssonii and P. auritus.     

Experimental evidence for group hunting via eavesdropping in echolocating bats

Group foraging has been suggested as an important factor for the evolution of sociality. However, visual cues are predominantly used to gain information about group members'' foraging success in diurnally foraging animals such as birds, where group foraging has been studied most intensively. By contrast, nocturnal animals, such as bats, would have to rely on other cues or signals to coordinate foraging. We investigated the role of echolocation calls as inadvertently produced cues for social foraging in the insectivorous bat Noctilio albiventris. Females of this species live in small groups, forage over water bodies for swarming insects and have an extremely short daily activity period. We predicted and confirmed that (i) free-ranging bats are attracted by playbacks of echolocation calls produced during prey capture, and that (ii) bats of the same social unit forage together to benefit from passive information transfer via the change in group members'' echolocation calls upon finding prey. Network analysis of high-resolution automated radio telemetry confirmed that group members flew within the predicted maximum hearing distance 94±6 per cent of the time. Thus, echolocation calls also serve as intraspecific communication cues. Sociality appears to allow for more effective group foraging strategies via eavesdropping on acoustical cues of group members in nocturnal mammals.     

Foraging shifts and visual preadaptation in ecologically diverse bats

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

Does body mass restrict call peak frequency in echolocating bats?

1. Echolocation is the ability of some animals to orient themselves through sound emission and interpretation of the echoes. This is bats’ main sense for orientation and recognising biotopes that provide food, water, and roosts. It is widely accepted that echolocation call frequency is related to body mass, and this relationship has been described as the ‘allometric hypothesis’, which proposes a negative correlation between these variables.
2. There is evidence that, in many cases, the allometric hypothesis does not apply. Additionally, studies supporting this hypothesis were done at the family level, resulting in a broad range of correlation values with r ranging from −0.36 to −0.76, and only insectivorous bats were included. Due to the notable exceptions and the lack of a quantitative synthesis of this hypothesis including all echolocating bats, we evaluated the allometric hypothesis of echolocation calls for this group.
3. Using a meta-analysis and phylogenetic generalised least-squares techniques, we evaluated the relationship between echolocation call peak frequency and the body mass of bats.
4. We found a negative relationship between body mass and echolocation call peak frequency for the 85 bat species that were included in our analysis (r = −0.3, p = 0.005). The relationship was consistent when we analysed the data at the insectivorous guild level, and in bats belonging to the families Vespertilionidae, Rhinolophidae, Emballonuridae, and the genus Myotis. However, the wide range of r values suggests that the strength of the relationship between peak frequency and body mass varies within the order Chiroptera.
5. Our results support the allometric hypothesis of sound production in echolocating bats. However, the low coefficient we found suggests that factors other than body mass may influence the peak frequency of echolocation calls produced by bats.

     

Foraging ecology and niche partitioning in orb-weaving spiders

Summary Foraging patterns were determined for three orbweaving spiders in several geographical locations varying in percent cover by herbaceous vegetation. Argiope trifasciata was the most common species in early successional habitats, while both Argiope aurantia and Araneus trifolium were more common in wetter, more herbaceous sites. Discriminant analysis revealed that web height selected for webs and body size were the variables that explained most of the variation among populations in foraging patterns. Argiope aurantia forages lowest in vegetation, A. trifasciata at intermediate heights, and A. trifolium near the top of the vegetation. The body size sequence is reversed.Web radius, spider size, and web height appear to explain much of the variation in abundance and size of prey in webs. Species foraging higher in the vegetation take more winged prey, while larger species foraging lower in the vegetation tend to take larger, jumping prey like acridids. Comparison of prey in webs with field estimates of potential prey suggests that orbweavers select large insect prey. Inferential evidence indicates that interspecific competition may be responsible for the divergence in foraging patterns among species reported here. However, field manipulative experiments have not yet indicated that competition among orb-weavers is severe.     

Life history,ecology and longevity in bats

The evolutionary theory of aging predicts that life span should decrease in response to the amount of mortality caused by extrinsic sources. Using this prediction, we selected six life history and ecological factors to use in a comparative analysis of longevity among 64 bat species. On average, the maximum recorded life span of a bat is 3.5 times greater than a non-flying placental mammal of similar size. Records of individuals surviving more than 30 years in the wild now exist for five species. Univariate and multivariate analyses of species data, as well as of phylogenetically independent contrasts obtained using a supertree of Chiroptera, reveal that bat life span significantly increases with hibernation, body mass and occasional cave use, but decreases with reproductive rate and is not influenced by diet, colony size or the source of the record. These results are largely consistent with extrinsic mortality risk acting as a determinant of bat longevity. Nevertheless, the strong association between life span and both reproductive rate and hibernation also suggests that bat longevity is strongly influenced by seasonal allocation of non-renewable resources to reproduction. We speculate that hibernation may provide a natural example of caloric restriction, which is known to increase longevity in other mammals.