Social information facilitates learning about novel food sources in adult flower-visiting bats.

Incorporating novel food sources into their diet is crucial for animals in changing environments. Although the utilization of novel food sources can be learned individually, learning socially from experienced conspecifics may facilitate this task and enable a transmission of foraging-related innovations across a population. In anthropogenically modified habitats, bats (Mammalia: Chiroptera) frequently adapt their feeding strategy to novel food sources, and corresponding social learning processes have been experimentally demonstrated in frugivorous and animalivorous species. However, comparable experiments are lacking for nectarivorous flower-visiting bats, even though their utilization of novel food sources in anthropogenically altered habitats is often observed and even discussed as the reason why bats are able to live in some areas. In the present study, we investigated whether adult flower-visiting bats may benefit from social information when learning about a novel food source. We conducted a demonstrator-observer dyad with wild Pallas' long-tongued bats (Glossophaga soricina; Phyllostomidae: Glossophaginae) and hypothesized that naïve individuals would learn to exploit a novel food source faster when accompanied by an experienced demonstrator bat. Our results support this hypothesis and demonstrate flower-visiting bats to be capable of using social information to expand their dietary repertoire.

Robust evidence for bats as reservoir hosts is lacking in most African virus studies: a review and call to optimize sampling and conserve bats.

Africa experiences frequent emerging disease outbreaks among humans, with bats often proposed as zoonotic pathogen hosts. We comprehensively reviewed virus-bat findings from papers published between 1978 and 2020 to evaluate the evidence that African bats are reservoir and/or bridging hosts for viruses that cause human disease. We present data from 162 papers (of 1322) with original findings on (1) numbers and species of bats sampled across bat families and the continent, (2) how bats were selected for study inclusion, (3) if bats were terminally sampled, (4) what types of ecological data, if any, were recorded and (5) which viruses were detected and with what methodology. We propose a scheme for evaluating presumed virus-host relationships by evidence type and quality, using the contrasting available evidence for Orthoebolavirus versus Orthomarburgvirus as an example. We review the wording in abstracts and discussions of all 162 papers, identifying key framing terms, how these refer to findings, and how they might contribute to people's beliefs about bats. We discuss the impact of scientific research communication on public perception and emphasize the need for strategies that minimize human-bat conflict and support bat conservation. Finally, we make recommendations for best practices that will improve virological study metadata.

Acoustic traits of bat-pollinated flowers compared to flowers of other pollination syndromes and their echo-based classification using convolutional neural networks.

Bat-pollinated flowers have to attract their pollinators in absence of light and therefore some species developed specialized echoic floral parts. These parts are usually concave shaped and act like acoustic retroreflectors making the flowers acoustically conspicuous to the bats. Acoustic plant specializations only have been described for two bat-pollinated species in the Neotropics and one other bat-dependent plant in South East Asia. However, it remains unclear whether other bat-pollinated plant species also show acoustic adaptations. Moreover, acoustic traits have never been compared between bat-pollinated flowers and flowers belonging to other pollination syndromes. To investigate acoustic traits of bat-pollinated flowers we recorded a dataset of 32320 flower echoes, collected from 168 individual flowers belonging to 12 different species. 6 of these species were pollinated by bats and 6 species were pollinated by insects or hummingbirds. We analyzed the spectral target strength of the flowers and trained a convolutional neural network (CNN) on the spectrograms of the flower echoes. We found that bat-pollinated flowers have a significantly higher echo target strength, independent of their size, and differ in their morphology, specifically in the lower variance of their morphological features. We found that a good classification accuracy by our CNN (up to 84%) can be achieved with only one echo/spectrogram to classify the 12 different plant species, both bat-pollinated and otherwise, with bat-pollinated flowers being easier to classify. The higher classification performance of bat-pollinated flowers can be explained by the lower variance of their morphology.

Hearing sensitivity and amplitude coding in bats are differentially shaped by echolocation calls and social calls.

Differences in auditory perception between species are influenced by phylogenetic origin and the perceptual challenges imposed by the natural environment, such as detecting prey- or predator-generated sounds and communication signals. Bats are well suited for comparative studies on auditory perception since they predominantly rely on echolocation to perceive the world, while their social calls and most environmental sounds have low frequencies. We tested if hearing sensitivity and stimulus level coding in bats differ between high and low-frequency ranges by measuring auditory brainstem responses (ABRs) of 86 bats belonging to 11 species. In most species, auditory sensitivity was equally good at both high- and low-frequency ranges, while amplitude was more finely coded for higher frequency ranges. Additionally, we conducted a phylogenetic comparative analysis by combining our ABR data with published data on 27 species. Species-specific peaks in hearing sensitivity correlated with peak frequencies of echolocation calls and pup isolation calls, suggesting that changes in hearing sensitivity evolved in response to frequency changes of echolocation and social calls. Overall, our study provides the most comprehensive comparative assessment of bat hearing capacities to date and highlights the evolutionary pressures acting on their sensory perception.

Comparison of methods for rhythm analysis of complex animals' acoustic signals.

Analyzing the rhythm of animals' acoustic signals is of interest to a growing number of researchers: evolutionary biologists want to disentangle how these structures evolved and what patterns can be found, and ecologists and conservation biologists aim to discriminate cryptic species on the basis of parameters of acoustic signals such as temporal structures. Temporal structures are also relevant for research on vocal production learning, a part of which is for the animal to learn a temporal structure. These structures, in other words, these rhythms, are the topic of this paper. How can they be investigated in a meaningful, comparable and universal way? Several approaches exist. Here we used five methods to compare their suitability and interpretability for different questions and datasets and test how they support the reproducibility of results and bypass biases. Three very different datasets with regards to recording situation, length and context were analyzed: two social vocalizations of Neotropical bats (multisyllabic, medium long isolation calls of Saccopteryx bilineata, and monosyllabic, very short isolation calls of Carollia perspicillata) and click trains of sperm whales, Physeter macrocephalus. Techniques to be compared included Fourier analysis with a newly developed goodness-of-fit value, a generate-and-test approach where data was overlaid with varying artificial beats, and the analysis of inter-onset-intervals and calculations of a normalized Pairwise Variability Index (nPVI). We discuss the advantages and disadvantages of the methods and we also show suggestions on how to best visualize rhythm analysis results. Furthermore, we developed a decision tree that will enable researchers to select a suitable and comparable method on the basis of their data.

The origins and diversity of bat songs.

Singing plays an important role in the social lives of several disparate bat species, but just how significant the behavior may be among bats generally is unknown. Recent discoveries suggest singing by bats might be surprisingly more diverse and widespread than anticipated, but if true then two questions must be addressed: firstly why has singing been so rarely documented among bats, and secondly do bats sing for the same reasons as songbirds? We address the first question by reviewing how sampling bias and technical constraints may have produced a myopic view of bat social communication. To address the second question, we review evidence from 50 years of batsong literature supporting the supposition that bat singing is linked to the same constellation of ecological variables that favored birdsong, including territoriality, polygyny, metabolic constraints, migratory behaviors and especially powered flight. We propose that bats sing like birds because they fly like birds; flight is energetically expensive and singing reduces time spent flying. Factoring in the singular importance of acoustic communication for echolocating bats, it seems likely that singing may prove to be relatively common among certain groups of bats once it becomes clear when and where to look for it.

Learning where to feed: the use of social information in flower-visiting Pallas' long-tongued bats (Glossophaga soricina).

Social learning is a widespread phenomenon among vertebrates that influences various patterns of behaviour and is often reported with respect to foraging behaviour. The use of social information by foraging bats was documented in insectivorous, carnivorous and frugivorous species, but there are little data whether flower-visiting nectarivorous bats (Phyllostomidae: Glossophaginae) can acquire information about food from other individuals. In this study, we conducted an experiment with a demonstrator-observer paradigm to investigate whether flower-visiting Pallas' long-tongued bats (Glossophaga soricina) are able to socially learn novel flower positions via observation of, or interaction with, knowledgeable conspecifics. The results demonstrate that flower-visiting G. soricina are able to use social information for the location of novel flower positions and can thereby reduce energy-costly search efforts. This social transmission is explainable as a result of local enhancement; learning bats might rely on both visual and echo-acoustical perception and are likely to eavesdrop on auditory cues that are emitted by feeding conspecifics. We additionally tested the spatial memory capacity of former demonstrator bats when retrieving a learned flower position, and the results indicate that flower-visiting bats remember a learned flower position after several weeks.

Calling to the collective: contact calling rates within groups of disc-winged bats do not vary by kinship or association.

Many group-living animals coordinate social behaviours using contact calls, which can be produced for all group members or targeted at specific individuals. In the disc-winged bat, Thyroptera tricolor, group members use 'inquiry' and 'response' calls to coordinate daily movements into new roosts (furled leaves). Rates of both calls show consistent among-individual variation, but causes of within-individual variation remain unknown. Here, we tested whether disc-winged bats produce more contact calls towards group members with higher kinship or association. In 446 experimental trials, we recorded 139 random within-group pairs of one flying bat (producing inquiry calls for roost searching) and one roosting bat (producing response calls for roost advertising). Using generalized linear mixed-effect models (GLMM), we assessed how response and inquiry calling rates varied by sender, receiver, genetic kinship and co-roosting association rate. Calling rates varied consistently across senders but not by receiver. Response calling was influenced by inquiry calling rates, but neither calling rate was higher when the interacting pair had higher kinship or association. Rather than dyadic calling rates indicating within-group relationships, our findings are consistent with the hypothesis that bats produce contact calls to maintain contact with any or all individuals within a group while collectively searching for a new roost site. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Highly diversified coronaviruses in neotropical bats.

Bats host a broad diversity of coronaviruses (CoVs), including close relatives of human pathogens. There is only limited data on neotropical bat CoVs. We analysed faecal, blood and intestine specimens from 1562 bats sampled in Costa Rica, Panama, Ecuador and Brazil for CoVs by broad-range PCR. CoV RNA was detected in 50 bats representing nine different species, both frugivorous and insectivorous. These bat CoVs were unrelated to known human or animal pathogens, indicating an absence of recent zoonotic spill-over events. Based on RNA-dependent RNA polymerase (RdRp)-based grouping units (RGUs) as a surrogate for CoV species identification, the 50 viruses represented five different alphacoronavirus RGUs and two betacoronavirus RGUs. Closely related alphacoronaviruses were detected in Carollia perspicillata and C. brevicauda across a geographical distance exceeding 5600 km. Our study expands the knowledge on CoV diversity in neotropical bats and emphasizes the association of distinct CoVs and bat host genera.

Female-biased dispersal in a bat with a female-defence mating strategy.

The ultimate causes for predominant male-biased dispersal (MBD) in mammals and female-biased dispersal (FBD) in birds are still subject to much debate. Studying exceptions to general patterns of dispersal, for example, FBD in mammals, provides a valuable opportunity to test the validity of proposed evolutionary pressures. We used long-term behavioural and genetic data on individually banded Proboscis bats (Rhynchonycteris naso) to show that this species is one of the rare mammalian exceptions with FBD. Our results suggest that all females disperse from their natal colonies prior to first reproduction and that a substantial proportion of males are philopatric and reproduce in their natal colonies, although male immigration has also been detected. The age of females at first conception falls below the tenure of males, suggesting that females disperse to avoid father-daughter inbreeding. Male philopatry in this species is intriguing because Proboscis bats do not share the usual mammalian correlates (i.e. resource-defence polygyny and/or kin cooperation) of male philopatry. They have a mating strategy based on female defence, where local mate competition between male kin is supposedly severe and should prevent the evolution of male philopatry. However, in contrast to immigrant males, philopatric males may profit from acquaintance with the natal foraging grounds and may be able to attain dominance easier and/or earlier in life. Our results on Proboscis bats lent additional support to the importance of inbreeding avoidance in shaping sex-biased dispersal patterns and suggest that resource defence by males or kin cooperation cannot fully explain the evolution of male philopatry in mammals.

Bat echolocation calls facilitate social communication.

Bat echolocation is primarily used for orientation and foraging but also holds great potential for social communication. The communicative function of echolocation calls is still largely unstudied, especially in the wild. Eavesdropping on vocal signatures encoding social information in echolocation calls has not, to our knowledge, been studied in free-living bats so far. We analysed echolocation calls of the polygynous bat Saccopteryx bilineata and found pronounced vocal signatures encoding sex and individual identity. We showed experimentally that free-living males discriminate approaching male and female conspecifics solely based on their echolocation calls. Males always produced aggressive vocalizations when hearing male echolocation calls and courtship vocalizations when hearing female echolocation calls; hence, they responded with complex social vocalizations in the appropriate social context. Our study demonstrates that social information encoded in bat echolocation calls plays a crucial and hitherto underestimated role for eavesdropping conspecifics and thus facilitates social communication in a highly mobile nocturnal mammal.

Morphological specialization influences nectar extraction efficiency of sympatric nectar-feeding bats.

Mammals frequently use nectar as a supplementary food, while a predominantly nectarivorous lifestyle with morphological specializations for this feeding mode is rare within the class. However, Neotropical flower-visiting bats largely depend on nectar resources and show distinct adaptations to a nectar diet. Glossophagine bats form local guilds of 2-6 species that may differ distinctly in skull morphology. It is still unknown how and to what extent this morphological diversity influences the efficiency of nectar extraction and hence resource partitioning within the local bat guild. As foraging behaviour is a key factor for niche partitioning of co-existing species, we compared nectar extraction behaviour and efficiency at different flower depths among sympatric bat species with different degrees of morphological specialization (Glossophaga soricina, Leptonycteris yerbabuenae and Musonycteris harrisoni). In flight cage experiments with artificial flowers, at deeper nectar levels all species showed a distinct decrease in the amount of nectar extracted per visit and an increase in the time spent hovering at the flower, indicating increased energetic cost when foraging on longer tubed flowers. The lowest nectar extraction efficiency (g s(-1)) was found in the small G. soricina and the highest in the largest species L. yerbabuenae. However, when also considering the different energy requirements of the different-sized bat species, the morphologically most specialized M. harrisoni consistently showed the highest foraging efficiency. Our data suggest that the long rostrum and tongue of the extremely specialized M. harrisoni are probably not evolved for monopolization of co-evolved deep flowers but for allowing efficient access to the broadest range of the local chiropterophilous flower resources.

The soundscape of swarming: Proof of concept for a noninvasive acoustic species identification of swarming Myotis bats.

Bats emit echolocation calls to orientate in their predominantly dark environment. Recording of species-specific calls can facilitate species identification, especially when mist netting is not feasible. However, some taxa, such as Myotis bats can be hard to distinguish acoustically. In crowded situations where calls of many individuals overlap, the subtle differences between species are additionally attenuated. Here, we sought to noninvasively study the phenology of Myotis bats during autumn swarming at a prominent hibernaculum. To do so, we recorded sequences of overlapping echolocation calls (N = 564) during nights of high swarming activity and extracted spectral parameters (peak frequency, start frequency, spectral centroid) and linear frequency cepstral coefficients (LFCCs), which additionally encompass the timbre (vocal "color") of calls. We used this parameter combination in a stepwise discriminant function analysis (DFA) to classify the call sequences to species level. A set of previously identified call sequences of single flying Myotis daubentonii and Myotis nattereri, the most common species at our study site, functioned as a training set for the DFA. 90.2% of the call sequences could be assigned to either M. daubentonii or M. nattereri, indicating the predominantly swarming species at the time of recording. We verified our results by correctly classifying the second set of previously identified call sequences with an accuracy of 100%. In addition, our acoustic species classification corresponds well to the existing knowledge on swarming phenology at the hibernaculum. Moreover, we successfully classified call sequences from a different hibernaculum to species level and verified our classification results by capturing swarming bats while we recorded them. Our findings provide a proof of concept for a new noninvasive acoustic monitoring technique that analyses "swarming soundscapes" by combining classical acoustic parameters and LFCCs, instead of analyzing single calls. Our approach for species identification is especially beneficial in situations with multiple calling individuals, such as autumn swarming.

Vocal production learning in mammals revisited.

Vocal production learning, the ability to modify the structure of vocalizations as a result of hearing those of others, has been studied extensively in birds but less attention has been given to its occurrence in mammals. We summarize the available evidence for vocal learning in mammals from the last 25 years, updating earlier reviews on the subject. The clearest evidence comes from cetaceans, pinnipeds, elephants and bats where species have been found to copy artificial or human language sounds, or match acoustic models of different sound types. Vocal convergence, in which parameter adjustments within one sound type result in similarities between individuals, occurs in a wider range of mammalian orders with additional evidence from primates, mole-rats, goats and mice. Currently, the underlying mechanisms for convergence are unclear with vocal production learning but also usage learning or matching physiological states being possible explanations. For experimental studies, we highlight the importance of quantitative comparisons of seemingly learned sounds with vocal repertoires before learning started or with species repertoires to confirm novelty. Further studies on the mammalian orders presented here as well as others are needed to explore learning skills and limitations in greater detail. This article is part of the theme issue 'Vocal learning in animals and humans'.

Novel ideas to further expand the applicability of rhythm analysis.

The temporal structure of animals' acoustic signals can inform about context, urgency, species, individual identity, or geographical origin. We present three independent ideas to further expand the applicability of rhythm analysis for isochronous, that is, metronome-like, rhythms. A description of a rhythm or beat needs to include a description of its goodness of fit, meaning how well the rhythm describes a sequence. Existing goodness-of-fit values are not comparable between methods and datasets. Furthermore, they are strongly correlated with certain parameters of the described sequence, for example, the number of elements in the sequence. We introduce a new universal goodness-of-fit value, ugof, comparable across methods and datasets, which illustrates how well a certain beat frequency in Hz describes the temporal structure of a sequence of elements. We then describe two additional approaches to adapt already existing methods to analyze the rhythm of acoustic sequences of animals. The new additions, a slightly modified way to use the already established Fourier analysis and concrete examples on how to use the visualization with recurrence plots, enable the analysis of more variable data, while giving more details than previously proposed measures. New methods are tested on 6 datasets including the very complex flight songs of male skylarks. The ugof is the first goodness-of-fit value capable of giving the information per element, instead of only per sequence. Advantages and possible interpretations of the new approaches are discussed. The new methods enable the analysis of more variable and complex communication signals. They give indications on which levels and structures to analyze and enable to track changes and differences in individuals or populations, for instance, during ontogeny or across regions. Especially, the ugof is not restricted to the analysis of acoustic signals but could for example also be applied on heartbeat measurements. Taken together, the ugof and proposed method additions greatly broaden the scope of rhythm analysis methods.

Babbling in a vocal learning bat resembles human infant babbling.

Babbling is a production milestone in infant speech development. Evidence for babbling in nonhuman mammals is scarce, which has prevented cross-species comparisons. In this study, we investigated the conspicuous babbling behavior of Saccopteryx bilineata, a bat capable of vocal production learning. We analyzed the babbling of 20 bat pups in the field during their 3-month ontogeny and compared its features to those that characterize babbling in human infants. Our findings demonstrate that babbling in bat pups is characterized by the same eight features as babbling in human infants, including the conspicuous features reduplication and rhythmicity. These parallels in vocal ontogeny between two mammalian species offer future possibilities for comparison of cognitive and neuromolecular mechanisms and adaptive functions of babbling in bats and humans.

Social behaviour and vocalizations of the tent-roosting Honduran white bat.

Bats are highly gregarious animals, displaying a large spectrum of social systems with different organizational structures. One important factor shaping sociality is group stability. To maintain group cohesion and stability, bats often rely on vocal communication. The Honduran white bat, Ectophylla alba, exhibits an unusual social structure compared to other tent-roosting species. This small white-furred bat lives in perennial stable mixed-sex groups. Tent construction requires several individuals and, as the only tent roosting species so far, involves both sexes. The bats´ social system and ecology render this species an interesting candidate to study social behaviour and vocal communication. In our study, we investigated the social behaviour and vocalizations of E. alba in the tent by observing two stable groups, including pups, in the wild. We documented 16 different behaviours, among others play and fur chewing, a behaviour presumably used for scent-marking. Moreover, we found 10 distinct social call types in addition to echolocation calls, and for seven call types we were able to identify the corresponding broad behavioural context. Most of the social call types were affiliative, including two types of contact calls, maternal directive calls, pup isolation calls and a call type related to the fur-chewing behaviour. In sum, this study entails an ethogram and describes the social vocalizations of a tent-roosting phyllostomid bat, providing the basis for further in-depth studies about the sociality and vocal communication in E. alba.

Cross-species parallels in babbling: animals and algorithms.

A key feature of vocal ontogeny in a variety of taxa with extensive vocal repertoires is a developmental pattern in which vocal exploration is followed by a period of category formation that results in a mature species-specific repertoire. Vocal development preceding the adult repertoire is often called 'babbling', a term used to describe aspects of vocal development in species of vocal-learning birds, some marine mammals, some New World monkeys, some bats and humans. The paper summarizes the results of research on babbling in examples from five taxa and proposes a unifying definition facilitating their comparison. There are notable similarities across these species in the developmental pattern of vocalizations, suggesting that vocal production learning might require babbling. However, the current state of the literature is insufficient to confirm this suggestion. We suggest directions for future research to elucidate this issue, emphasizing the importance of (i) expanding the descriptive data and seeking species with complex mature repertoires where babbling may not occur or may occur only to a minimal extent; (ii) (quasi-)experimental research to tease apart possible mechanisms of acquisition and/or self-organizing development; and (iii) computational modelling as a methodology to test hypotheses about the origins and functions of babbling. This article is part of the theme issue 'Vocal learning in animals and humans'.

DNA methylation predicts age and provides insight into exceptional longevity of bats.

Exceptionally long-lived species, including many bats, rarely show overt signs of aging, making it difficult to determine why species differ in lifespan. Here, we use DNA methylation (DNAm) profiles from 712 known-age bats, representing 26 species, to identify epigenetic changes associated with age and longevity. We demonstrate that DNAm accurately predicts chronological age. Across species, longevity is negatively associated with the rate of DNAm change at age-associated sites. Furthermore, analysis of several bat genomes reveals that hypermethylated age- and longevity-associated sites are disproportionately located in promoter regions of key transcription factors (TF) and enriched for histone and chromatin features associated with transcriptional regulation. Predicted TF binding site motifs and enrichment analyses indicate that age-related methylation change is influenced by developmental processes, while longevity-related DNAm change is associated with innate immunity or tumorigenesis genes, suggesting that bat longevity results from augmented immune response and cancer suppression.

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.