Bat Calls Research Articles

Neural representation of bat predation risk and evasive flight in moths: A modelling approach

Most animals are at risk from multiple predators and can vary anti-predator behaviour based on the level of threat posed by each predator. Animals use sensory systems to detect predator cues, but the relationship between the tuning of sensory systems and the sensory cues related to predator threat are not well-studied at the community level. Noctuid moths have ultrasound-sensitive ears to detect the echolocation calls of predatory bats. Here, combining empirical data and mathematical modelling, we show that moth hearing is adapted to provide information about the threat posed by different sympatric bat species. First, we found that multiple characteristics related to the threat posed by bats to moths correlate with bat echolocation call frequency. Second, the frequency tuning of the most sensitive auditory receptor in noctuid moth ears provides information allowing moths to escape detection by all sympatric bats with similar safety margin distances. Third, the least sensitive auditory receptor usually responds to bat echolocation calls at a similar distance across all moth species for a given bat species. If this neuron triggers last-ditch evasive flight, it suggests that there is an ideal reaction distance for each bat species, regardless of moth size. This study shows that even a very simple sensory system can adapt to deliver information suitable for triggering appropriate defensive reactions to each predator in a multiple predator community.

Echolocation call divergence in bats: a comparative analysis

Animal vocalizations experience pressures from ecological conditions, but their diversification may be constrained by morphology and evolutionary history. To date, the relative contribution of these factors to acoustic diversity is unclear in most vertebrate groups. Bats constitute one of the most speciose and diverse mammal groups, and most bat species rely on vocalizations for orientation, foraging, and communication. Here, we examine echolocation calls of 207 bat species across 17 families to weigh the relative role of phylogenetic inertia, natural selection, and morphological constraints in shaping echolocation call diversity in bats. Using the large dataset, we confirm that foraging guilds, phylogenetic relationships, and forearm length account for the majority of the variation in call parameters among bats. Foraging guilds play a major role in influencing call parameters in low duty cycle bats. At the family level, the variation in call parameters is primarily explained by differences in body size and phylogenetic relationships. Path analyses indicate that phylogeny determines call output not only by their direct effect on call parameters but also by having an indirect effect via foraging guilds and body size. These results demonstrate that natural selection, phylogenetic constraint, and morphological constraint shape echolocation call divergence in bats. Our findings underscore the importance of both adaptive and non-adaptive mechanisms underlying the evolution of echolocation calls in bats. Ecology, morphology, and evolutionary history are tightly coupled; therefore, disentangling the relative strength of these components underlying acoustic diversity is a big challenge. Using a large dataset of bats, we assess the influence of phylogeny, ecology, and body size on echolocation call parameters. We conclude that ecological selection, phylogenetic constraint, and morphological constraint play a crucial role in shaping echolocation call divergence among bats. This study expands our knowledge of the relative contribution of adaptive and maladaptive mechanisms to echolocation call diversity at different taxonomic levels in bats.

Species Richness and Seasonality of Bat Occupancy on Northwestern National Wildlife Refuges

Abstract Bats are critical to ecosystem integrity but are being threatened by a variety of disease and anthropogenic stressors. Further, information is generally lacking on basic parameters necessary for long-term bat conservation in North America, including the timing of seasonal activity and location of overwintering sites. Between 2011 and 2016, we used passive acoustic recording equipment to collect and analyze 115,855 bat calls from six National Wildlife Refuges across three geographic areas in the northwestern United States; the majority of the data was collected from 2014 to 2015. We documented the presence of 16 species, with species richness varying from 6 to 15 species across sampled Refuges. This includes detection of two species outside of their expected ranges: western red bat Lasiurus blossevillii were found in the Great Basin and western pipistrelle Pipistrellus hysperus were found in the Northern Rockies. Overwintering bats were found across all three geographic areas, although only one species, western pipistrelle, was documented as active year round on more than one Refuge. Six species of bats were also identified as potentially overwintering within their respective areas. For suspected nonoverwintering species, including those considered susceptible to white-nose syndrome, dates of first detections began in early March to early May and last detections between early October and early November. Public lands established for conservation can provide important monitoring and conservation resources for bats.

Loudness–Duration Tradeoff in Ultrasonic Courtship Songs of Moths

Moths have evolved auditory channels under predation pressure from insectivorous bats that emit ultrasonic pulses for capturing prey, including moths. Tympanate moths perform evasive behavior in response to echolocation calls of bats, but they also utilize ultrasonic signals mostly generated by males close to an intended female mate in the context of courtship. Unlike calling songs used to advertise the presence and sexual attractiveness of the signaler, courtship songs need not always be acoustically conspicuous. Male courtship songs are predominantly soft but sufficient for detection by a nearby potential mate. Quiet courtship songs are thought to effectively avoid being eavesdropped by gleaning bats, acoustic parasitoids, and conspecific competitors, i.e., rival males. However, males of some moth species generate loud courtship songs. In the present study, the duration of courtship song, in addition to the sound level of the song was predicted to affect the likelihood of being perceived by eavesdroppers. Loud and lengthy courtship songs, which are easily exploited by eavesdroppers, would be expected to rarely evolve, because a female receiver close to a male emitting a conspicuous song would also be exposed to strong predation pressure. This study explored the relationship between the peak sound level and the duration of single song bouts in 26 moth species from the following families: Noctuidae, Erebidae, Crambidae, Pyralidae, and Geometridae. The softest and loudest songs with mean peak sound levels of 64 and 129dB peSPL had mean durations of 1900 and 312 ms, respectively, whereas the shortest and longest songs with mean durations of 110 and 8839 ms had mean peak sound levels of 102 and 74 dB peSPL, respectively. Thus, the peak sound level and duration of courtship song exhibited a significant negative relationship. Although the energetic cost of producing song and the size of the sound-producing organ might also affect the relationship, the data support the conclusion that acoustic moths have adaptively evolved ultrasonic courtship songs with properties between “soft-and-long” and “loud-and-short” to avoid eavesdroppers.

Let's Agree to Disagree: Comparing Auto-Acoustic Identification Programs for Northeastern Bats

Abstract With the declines in abundance and changing distribution of white-nose syndrome–affected bat species, increased reliance on acoustic monitoring is now the new “normal.” As such, the ability to accurately identify individual bat species with acoustic identification programs has become increasingly important. We assessed rates of disagreement between the three U.S. Fish and Wildlife Service–approved acoustic identification software programs (Kaleidoscope Pro 4.2.0, Echoclass 3.1, and Bat Call Identification 2.7d) and manual visual identification using acoustic data collected during summers from 2003 to 2017 at Fort Drum, New York. We assessed the percentage of agreement between programs through pairwise comparisons on a total nightly count level, individual file level (e.g., individual echolocation pass call file), and grouped maximum likelihood estimate level (e.g., probability values that a species is misclassified as present when in fact it is absent) using preplanned contrasts, Akaike Information Criterion, and annual confusion matrices. Interprogram agreement on an individual file level was low, as measured by Cohen's Kappa (0.2–0.6). However, site-night level pairwise comparative analysis indicated that program agreement was higher (40–90%) using single season occupancy metrics. In comparing analytical outcomes of our different datasets (i.e., how comparable programs and visual identification are regarding the relationship between environmental conditions and bat activity), we determined high levels of congruency in the relative rankings of the model as well as the relative level of support for each individual model. This indicated that among individual software packages, when analyzing bat calls, there was consistent ecological inference beyond the file-by-file level at the scales used by managers. Depending on objectives, we believe our results can help users choose automated software and maximum likelihood estimate thresholds more appropriate for their needs and allow for better cross-comparison of studies using different automated acoustic software.

Social signatures in echolocation calls of a leaf-roosting bat, Kerivoula furva

ABSTRACT Bats may use echolocation for social communication (e.g. group cohesion and individual recognition) although it has evolved primarily for orientation and foraging. This idea has been tested by using bats living in permanent roosts (e.g. caves) in large colonies. Here, we investigated social signatures in echolocation calls of a leaf-roosting bat, Kerivoula furva, which forms a small-sized group (2–10 individuals), roosts in furled banana leaves and switches roosts almost every day following foliation, but nevertheless, its group membership is largely fixed. We hypothesised that echolocation calls of K. furva differ significantly between groups and/or individuals, so that individuals can effectively find roost members, despite frequently changing roosts. Social structural and call analyses supported this hypothesis. Discriminant function analysis provided correct classifications significantly better than random ones, with 34.8% vs. 25% and 26.5% vs. 6.25% for group and individual signatures, respectively. Taken together with previous studies, our results suggest the possibility that, irrespective of the roost type, echolocation calls of bats generally contain enough information to be potentially useful for social communication. Future studies are encouraged to accumulate individual call data for a standardized comparison of context-dependent call signatures and to better understand social communication of bats.

Bat sonar and wing morphology predict species vertical niche.

The use of echolocation allows insectivorous bats to access unique foraging niches by locating obstacles and prey with ultrasounds in complete darkness. To avoid interspecific competition, it is likely that sonar features and wing morphology co-evolved with species vertical distribution, but due to the technical difficulties of studying flight in the vertical dimension, this has never been demonstrated with empirical measurements. The authors equipped 48 wind masts with arrays of two microphones and located the vertical distribution of a community of 19 bat species and two species groups over their annual activity period (>8000 nights). The authors tested the correlation between the proportion of flights at height and the acoustic features of bat calls as well as their wing morphology. The authors found that call peak frequency and bandwidth are good predictors of bat use of the vertical space regardless of their acoustic strategies (i.e., gleaning, hawking, or detecting prey flutter). High wing aspect ratios and high wing loadings were associated with high proportions of time spent at height, confirming hypotheses from the literature.

Major roads have important negative effects on insectivorous bat activity

The development of transportation infrastructure has been identified as one of the main pressures on biodiversity. The effects of transport infrastructure are more documented for terrestrial mammals, birds and amphibians than for bats. To assess the impacts of roads on bat activity, we carried out full-night acoustic recordings of bat calls at 306 sampling points at different distances from a major road at three study sites in France. To assess the relationship between bat activity and the distance to the major road, we performed generalized linear mixed model analyses for thirteen different species or groups and additionally explored the non-linear effect with generalized additive mixed models. Our results showed that low-flying species are more affected than high-flying species. Indeed, we found a significant negative effect of major roads on bat activity for the ‘clutter-adapted’ species, Eptesicus serotinus, Myotis spp., Pipistrellus pipistrellus and Rhinolophus hipposideros. These results demonstrate that the road-effect zone of major roads extends up to five kilometres. Extrapolating those road-effects zones to the major roads in the European Union, we estimated that 35% of the European Union is potentially negatively impacted. Finally, it seems urgent to consider these road effects with the cumulative effects of other roads by improving habitat connectivity and foraging areas in land use policies. Additionally, to implement drastic conservation practices for species of conservation concern in environmental impact assessment studies, efficient mitigation and offset measures implemented should be sized proportionally to the disturbance caused.

Bat Pass Duration Measurement: An Indirect Measure of Distance of Detection

Few reports have been published on detection distances of bat calls because the evaluation of detection distance is complicated. Several of the approaches used to measure detection distances are based on the researcher’s experience and judgment. More recently, multiple microphones have been used to model flight path. In this study, the validity of a low-cost and simple detectability metric was tested. We hypothesize that the duration of an echolocating-bat-pass within the area of an ultrasonic bat detector is correlated with the distance of detection. Two independent datasets from a large-scale acoustic bat survey—a total of 25,786 bat-passes from 20 taxa (18 species and two genera)—were measured. We found a strong relationship between these measures of bat-pass duration and published detection distances. The advantages of bat-pass duration measures are that, for each study, experimenters easily produce their own proxy for the distance of detection. This indirect measure of the distance of detection could be mobilized to monitor the loss in microphone sensitivity used to monitor long-term population trends. Finally, the possibility of producing an index for distance of detection provides a weight for each bat species’ activity when they are aggregated to produce a bat community metric, such as the widely used “total activity”.

Influence of vegetation and abiotic factors on habitat use by insectivorous bats in subtropical mountain forests

Forest structure and abiotic factors influence the habitat use of many mammals. For insectivorous bats, characteristics such as plant density, canopy cover, temperature, relative humidity and other seasonal changes over the course of the year can be important as regulators of food resource accessibility, and consequently of their nutritional health. The aim of this study was to determine the influence of the structure in two different forest types and of two abiotic factors, temperature and relative humidity, on habitat use by insectivorous bats in forests that present relatively small seasonal phenological changes. Sampling was conducted with ultrasonic detectors and the resulting recordings were used to analyse bat calls for identification of species and determination of bat activity. We found significant differences among the relative activities of the study species in both vegetation types. There was a tendency towards a greater increase in activity throughout the year in forests with either greater canopy cover or higher plant density. We found a positive correlation between temperature and activity in most of the recorded species, and a negative correlation between relative humidity and this activity. Our results show that relative humidity seems to be more influential than temperature on the activity patterns of insectivorous bats. Attenuation and its consequences could be more important to habitat use than heat loss in temperate subtropical forests (both cloud forest and pine forest).

Prolonged Bat Call Exposure Induces a Broad Transcriptional Response in the Male Fall Armyworm (Spodoptera frugiperda; Lepidoptera: Noctuidae) Brain.

Predation risk induces broad behavioral and physiological responses that have traditionally been considered acute and transitory. However, prolonged or frequent exposure to predators and the sensory cues of their presence they broadcast to the environment impact long-term prey physiology and demographics. Though several studies have assessed acute and chronic stress responses in varied taxa, these attempts have often involved a priori expectations of the molecular pathways involved in physiological responses, such as glucocorticoid pathways and neurohormone production in vertebrates. While relatively little is known about physiological and molecular predator-induced stress in insects, many dramatic insect defensive behaviors have evolved to combat selection by predators. For instance, several moth families, such as Noctuidae, include members equipped with tympanic organs that allow the perception of ultrasonic bat calls and facilitate predation avoidance by eliciting evasive aerial flight maneuvers. In this study, we exposed adult male fall armyworm (Spodoptera frugiperda) moths to recorded ultrasonic bat foraging and attack calls for a prolonged period and constructed a de novo transcriptome based on brain tissue from predator cue-exposed relative to control moths kept in silence. Differential expression analysis revealed that 290 transcripts were highly up- or down-regulated among treatment tissues, with many annotating to noteworthy proteins, including a heat shock protein and an antioxidant enzyme involved in cellular stress. Though nearly 50% of differentially expressed transcripts were unannotated, those that were are implied in a broad range of cellular functions within the insect brain, including neurotransmitter metabolism, ionotropic receptor expression, mitochondrial metabolism, heat shock protein activity, antioxidant enzyme activity, actin cytoskeleton dynamics, chromatin binding, methylation, axonal guidance, cilia development, and several signaling pathways. The five most significantly overrepresented Gene Ontology terms included chromatin binding, macromolecular complex binding, glutamate synthase activity, glutamate metabolic process, and glutamate biosynthetic process. As a first assessment of transcriptional responses to ecologically relevant auditory predator cues in the brain of moth prey, this study lays the foundation for examining the influence of these differentially expressed transcripts on insect behavior, physiology, and life history within the framework of predation risk, as observed in ultrasound-sensitive Lepidoptera and other ‘eared’ insects.

Function of Distress Calls in Least Horseshoe Bats: A Field Study Using Playback Experiments

Many social animals utter distress calls in the context of fear. These vocalizations may serve to attract audiences for help, warn individuals of danger, and confuse the predator. Here, we aim to assess the function of distress calls in free-living least horseshoe bats, Rhinolophus pusillus. We recorded distress calls from four allopatric colonies in mainland China. Playback trials, consisting of distress calls, silence, and noise, were presented to bats outside three bat roosts. Rhinolophus pusillus emitted long, harsh, broadband calls when under duress. Playback of distress calls induced a significant increase in bat passes at the loudspeaker in comparison with control trials. The number of recorded echolocation pulses increased 3.2–6.1 folds during playbacks of distress calls compared to playbacks of silence, and 2.9–5.2 folds compared to playbacks of noise. There was a positive association between bat passes and echolocation vocalizations. However, some bats delayed their emergence from the roost in response to distress call stimuli. Despite similar delayed responses, more bat passes were detected in the presence of allopatric distress calls than those from colony members. Overall, the results indicate that distress calls could attract and warn conspecifics in least horseshoe bats.

Navigation: from animal behaviour to guiding principles

![Figure][1] Tritonia diomedea navigating through a sea pen bed in search of prey or mates. Photo credit: Russell Wyeth and James A. Murray. Whether an animal's world is restricted to a few twigs or the avian highways that traverse the planet, creatures must navigate their surroundings

The number of bat calls per day in the winter season over two years in the urban arears of Kochi Prefecture, Shikoku, Japan

The number of bat calls per day in the winter season over two years in the urban arears of Kochi Prefecture, Shikoku, Japan

Responses of Short-Nosed Fruit Bat, <i>Cynopterus sphinx</i> (Vahl 1797) Towards Distress Calls of their Conspecifics from Related and Unrelated Sites:Implications for Building a Social Relationship

Distress calls emitted by bats signal their conspecifics either to warn them or inform them about the situations. Conspecifics may also get attracted towards distress calls as a behaviour of cooperative mobbing or just selfishly assessing the potential source of danger. The exact functions of distress calls in bats therefore vary to a great degree and are very hard to pinpoint. We conducted playback experiments to test the response of short-nosed fruit bat, Cynopterus sphinx towards the distress calls of their conspecifics from related and unrelated sites. Bats were attracted to their conspecifics from both related and unrelated sites and in one occasion towards fruit bat ( Rousettus leschenaulti ) of another genus within the same family. The response towards the opposite sex was significant in most of the playback trials and the reasons remain unclear. This symmetric response towards conspecifics from related and unrelated sites suggests the possibility of fruit bats building social relationships among unrelated individuals and probably between species.

Acoustic similarity elicits responses to heterospecific distress calls in bats (Mammalia: Chiroptera)

Frequently, individuals of one species respond to alarm calls produced by another species. This form of interspecies communication can be critical for survival. How animals recognize and respond to heterospecific alarm calls is, however, still poorly understood. This is especially true for bats, which are highly vocal and possess a specialized auditory system. We hypothesized that, among bat species, acoustic similarity between heterospecific and conspecific alarm calls is a key factor that underlies call recognition. However, this ability could also be acquired via associative learning from prior exposure or result from phylogenetic relatedness among caller and receiver species, as shown by others. Here we focused on distress calls of bats as representing a certain type of alarm call. To test our hypothesis, we recorded distress calls of 11 bat species from four families at five different sites. We broadcast the recorded calls to three of these species (Rhinolophus sinicus, Myotis badius and Myotis laniger). For all three species, neither prior exposure (familiarity) nor phylogenetic relatedness explained the variation in the response strength, as measured by echolocation vocalizations of receiver species in response to playback of heterospecific distress calls. In contrast, acoustic similarity, especially in peak frequency, between conspecific and heterospecific distress calls, was positively correlated with response strength in the receiver species. Thus, our findings emphasize that, at least among bats, acoustic similarity is a key factor allowing recognition of heterospecific alarm calls. It remains unclear whether evolutionary, genetic and/or neurophysiological mechanisms entrain an individual to respond selectively to a specific acoustic feature.

Stronger together: Combining automated classifiers with manual post-validation optimizes the workload vs reliability trade-off of species identification in bat acoustic surveys

Owing to major technological advances, bioacoustics has become a burgeoning field in ecological research worldwide. Autonomous passive acoustic recorders are becoming widely used to monitor aerial insectivorous bats, and automatic classifiers have emerged to aid researchers in the daunting task of analysing the resulting massive acoustic datasets. However, the scarcity of comprehensive reference call libraries still hampers their wider application in highly diverse tropical assemblages. Capitalizing on a unique acoustic dataset of >650,000 bat call sequences collected over a 3-year period in the Brazilian Amazon, the aims of this study were (a) to assess how pre-identified recordings of free-flying and hand-released bats could be used to train an automatic classification algorithm (random forest), and (b) to optimize acoustic analysis protocols by combining automatic classification with visual post-validation, whereby we evaluated the proportion of sound files to be post-validated for different thresholds of classification accuracy. Classifiers were trained at species or sonotype (group of species with similar calls) level. Random forest models confirmed the reliability of using calls of both free-flying and hand-released bats to train custom-built automatic classifiers. To achieve a general classification accuracy of ~85%, random forest had to be trained with at least 500 pulses per species/sonotype. For seven out of 20 sonotypes, the most abundant in our dataset, we obtained high classification accuracy (>90%). Adopting a desired accuracy probability threshold of 95% for the random forest classifier, we found that the percentage of sound files required for manual post-validation could be reduced by up to 75%, a significant saving in terms of workload. Combining automatic classification with manual ID through fully customizable classifiers implemented in open-source software as demonstrated here shows great potential to help overcome the acknowledged risks and biases associated with the sole reliance on automatic classification.

Illuminating the physiological implications of artificial light on an insectivorous bat community

Global light pollution threatens to disturb numerous wildlife species, but impacts of artificial light will likely vary among species within a community. Thus, artificial lights may change the environment in such a way as to create winners and losers as some species benefit while others do not. Insectivorous bats are nocturnal and a good model to test for differential effects of light pollution on a single community. We used a physiological technique to address this community-level question by measuring plasma ß-hydroxybutyrate (a blood metabolite) concentrations from six species of insectivorous bats in lit and unlit conditions. We also recorded bat calls acoustically to measure activity levels between experimental conditions. Blood metabolite level and acoustic activity data suggest species-specific changes in foraging around lights. In red bats (Lasiurus borealis), ß-hydroxybutyrate levels at lit sites were highest early in the night before decreasing. Acoustic data indicate pronounced peaks in activity at lit sites early in the night. In red bats on dark nights and in the other species in this community, which seem to avoid lights, ß-hydroxybutyrate remained relatively constant. Our results suggest red bats are more willing to expend energy to actively forage around lights despite potential negative impacts, while other, generally rarer species avoid lit areas. Artificial light appears to have a bifurcating effect on bat communities, whereby some species take advantage of concentrated prey resources, yet most do not. Further, this may concentrate light-intolerant species into limited dark refugia, thereby increasing competition for depauperate, phototactic insect communities.

Stealthy moths avoid bats with acoustic camouflage

Intense predation pressure from echolocating bats has led to the evolution of a host of anti-bat defences in nocturnal moths. Some have evolved ears to detect the ultrasonic biosonar of bats, yet there are many moths that are completely deaf. To enhance their survival chances, deaf moths must instead rely on passive defences. Here, we show that furry morphological specializations give moth bodies and wing joints acoustic stealth by reducing their echoes from bat calls. Using acoustic tomography, echo strength was quantified in the spatial and frequency domains of two deaf moth species that are subject to bat predation and two butterfly species that are not. Thoracic fur determines acoustic camouflage of moths but not butterflies. Thoracic fur provides substantial acoustic stealth at all ecologically relevant ultrasonic frequencies, with fur removal increasing a moth’s detection risk by as much as 38%. The thorax fur of moths acts as a lightweight porous sound absorber, facilitating acoustic camouflage and offering a significant survival advantage against bats.

Estimating population densities of temperate, insectivorous bats based on automatically recorded calls

Estimating population density based on automatically recorded calls is a key topic in bioacoustics, as individual recognition of animals is impossible. Several recently developed models do not require individual recognition but nevertheless allow to estimate density. However, there is a need to test these models on empirical data. Here, we used generalized random encounter models (gREM) to estimate population densities based on automatically recorded bat calls. To check the validity of the derived estimates, we fit Royle-Nichols models to species detection/non-detection data. Estimates of the two models were compared to each other and to estimates from published studies. The estimates of both models and literature estimates were within the same order of magnitude. Both models give reliable estimates of population density. However, we provide some cautionary notes for practical use: Bats which enter the detection sphere from above might bias results of gREMs, as the model simplifies the detection sphere to a two-dimensional area. On the other hand, reduction to detection/non-detection data in Royle-Nichols models results in information loss, which could limit their applicability in common species. Finally, we recommend to consider species behaviour carefully when applying one of the tested models.Estimating population density based on automatically recorded calls is a key topic in bioacoustics, as individual recognition of animals is impossible. Several recently developed models do not require individual recognition but nevertheless allow to estimate density. However, there is a need to test these models on empirical data. Here, we used generalized random encounter models (gREM) to estimate population densities based on automatically recorded bat calls. To check the validity of the derived estimates, we fit Royle-Nichols models to species detection/non-detection data. Estimates of the two models were compared to each other and to estimates from published studies. The estimates of both models and literature estimates were within the same order of magnitude. Both models give reliable estimates of population density. However, we provide some cautionary notes for practical use: Bats which enter the detection sphere from above might bias results of gREMs, as the model simplifies the detection sphere to...