Cortical representation of group social communication in bats.

Social interactions occur in group settings and are mediated by communication signals that are exchanged between individuals, often using vocalizations. The neural representation of group social communication remains largely unexplored. We conducted simultaneous wireless electrophysiological recordings from the frontal cortices of groups of Egyptian fruit bats engaged in both spontaneous and task-induced vocal interactions. We found that the activity of single neurons distinguished between vocalizations produced by self and by others, as well as among specific individuals. Coordinated neural activity among group members exhibited stable bidirectional interbrain correlation patterns specific to spontaneous communicative interactions. Tracking social and spatial arrangements within a group revealed a relationship between social preferences and intra- and interbrain activity patterns. Combined, these findings reveal a dedicated neural repertoire for group social communication within and across the brains of freely communicating groups of bats.

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.

Bats Out of Africa: Disentangling the Systematic Position and Biogeography of Bats in Cabo Verde.

Cabo Verde Archipelago presents one of the largest knowledge gaps in the distribution and taxonomy of bats in the world. Old works indicated that there are five species classified as European taxa. We have conducted an integrative taxonomy to revise the systematic position and distribution of Cabo Verdean bats with molecular, morphological, and ecological data, to test their native or exotic origin, and infer possible colonization patterns based on fieldwork and museum samples. Results showed that Cabo Verde Hypsugo is closely related to those from the Canary Islands, in which the taxonomic status is under debate, presenting unique mitochondrial and nuclear haplotypes. We also expanded the distribution of Taphozous nudiventris for Fogo Island through pellets and acoustic identification, showed unique haplotypes for this species, and that Miniopterus schreibersii shared a haplotype with European, North African, and Western Asian specimens. The morphological and acoustic identification of Cabo Verdean specimens was challenging because of the lack of modern morphological descriptions and similarity of echolocation calls within the same genus. More studies are definitely needed to access the systematic of bat species in the archipelago, but this work is the first step for the establishment of conservation actions of the probable only native Cabo Verdean mammals.

Development of New Food-Sharing Relationships in Vampire Bats.

Some nonhuman animals form adaptive long-term cooperative relationships with nonkin that seem analogous in form and function to human friendship [1-4]. However, it remains unclear how these bonds initially form, especially when they entail investments of time and energy. Theory suggests individuals can reduce the risk of exploitation by initially spreading out smaller cooperative investments across time [e.g., 5] or partners [6], then gradually escalating investments in more cooperative partnerships [7]. Despite its intuitive appeal, this raising-the-stakes model [7] has gained surprisingly scarce empirical support. Although human strangers do "raise the stakes" when making bids in cooperation games [8], there has been no clear evidence for raising the stakes during formation of social bonds in nature. Existing studies are limited to cooperative interactions with severe power asymmetries (e.g., the cleaner-client fish mutualism [9]) or snapshots of a single behavior within established relationships (grooming in primates [10-13]). Raising the stakes during relationship formation might involve escalating to more costly behaviors. For example, individuals could "test the waters" by first clustering for warmth (no cost), then conditionally grooming (low cost), and eventually providing coalitionary support (high cost). Detecting such a pattern requires introducing random strangers and measuring the emergence of natural helping behaviors that vary in costs. We performed this test by tracking the emergence of social grooming and regurgitated food donations among previously unfamiliar captive vampire bats (Desmodus rotundus) over 15 months. We found compelling evidence that vampire bats selectively escalate low-cost grooming before developing higher-cost food-sharing relationships.

Variability in the rigid pinna motions of hipposiderid bats and their impact on sensory information encoding.

Many bat species, e.g., in the rhinolophid and hipposiderid families, have dynamic biosonar systems with highly mobile pinnae. Pinna motion patterns have been shown to fall into two distinct categories: rigid rotations and non-rigid motions (i.e., deformations). In the present work, two questions regarding the rigid rotations have been investigated: (i) what is the nature of the variability (e.g., discrete subgroups or continuous variation) within the rigid motions, (ii) what is its acoustic impact? To investigate the first question, rigid pinna motions in Pratt's leaf-nosed bats (Hipposideros pratti) have been tracked with stereo vision and a dense set of landmark points on the pinna surface. Axis-angle representations of the recorded rigid motions have shown a continuous variation in the rotation axes that covered a range of almost 180° in azimuth and elevation. To investigate the second question, the observed range of rigid pinna motions has been reproduced with a biomimetic pinna. Normalized mutual information between acoustic inputs associated with every pair of the rigid pinna motions showed that even small changes in the rotation axis resulted in more than 50% new sensory information encoding capacity (i.e., normalized mutual information less than 50%). This demonstrates a potential sensory benefit to the observed variability in the rigid pinna rotations.

Mating strategy is determinant of adenovirus prevalence in European bats.

Adenoviruses are double-strained DNA viruses found in a great number of vertebrates, including humans. In order to understand their transmission dynamics, it is crucial, even from a human health perspective, to investigate how host traits influence their prevalence. Bats are important reservoirs for adenoviruses, and here we use the results of recent screenings in Western Europe to evaluate the association between characteristic traits of bat species and their probability of hosting adenoviruses, taking into account their phylogenetic relationships. Across species, we found an important phylogenetic component in the presence of adenoviruses and mating strategy as the most determinant factor conditioning the prevalence of adenoviruses across bat species. Contrary to other more stable mating strategies (e.g. harems), swarming could hinder transmission of adenoviruses since this strategy implies that contacts between individuals are too short. Alternatively, bat species with more promiscuous behavior may develop a stronger immune system. Outstandingly high prevalence of adenoviruses was reported for the Iberian species Pipistrellus pygmaeus, P. kuhlii and Nyctalus lasiopterus and we found that in the latter, males were more likely to be infected by adenoviruses than females, due to the immunosuppressing consequence of testosterone during the mating season. As a general trend across species, we found that the number of adenoviruses positive individuals was different across localities and that the difference in prevalence between populations was correlated with their geographic distances for two of the three studied bat species (P. pygmaeus and P.kuhlii). These results increase our knowledge about the transmission mechanisms of adenoviruses.

Big brown bats are challenged by acoustically-guided flights through a circular tunnel of hoops.

Mines and caves provide essential roosting places for bats, but often they are obstructed to prevent entry by humans. To allow bats to access their roosts, metal corrugated culvert pipes are sometimes installed. Wildlife surveys indicate, however, that bats may abandon caves having corrugated culvert entrances. Culverts may be confusing to bats due to the complex patterns of echoes returned by the regular, ring-like corrugations. We tested the hypothesis that a circular tunnel composed of successive hoops is difficult for big brown bats (Eptesicus fuscus) to navigate. Experiments challenged bats with flights through a tunnel of round plastic hoops or a corridor flanked left and right by rows of plastic hanging chains. The bats swerved sideways and left the pathway on more flights in the hoop tunnel compared to only rarely in the chain corridor. Even during successful flights through the hoops, bats changed the temporal patterning of their echolocation pulses to compress them into more sonar sound groups. From prior research, this active reaction is an indicator of a perceptually more difficult task. To allow bats access to mines through culverts without affecting their echolocation behavior, smoothing or masking the regular corrugations inside with concrete may be effective.

Avoidance of non-localizable obstacles in echolocating bats: A robotic model.

Most objects and vegetation making up the habitats of echolocating bats return a multitude of overlapping echoes. Recent evidence suggests that the limited temporal and spatial resolution of bio-sonar prevents bats from separately perceiving the objects giving rise to these overlapping echoes. Therefore, bats often operate under conditions where their ability to localize obstacles is severely limited. Nevertheless, bats excel at avoiding complex obstacles. In this paper, we present a robotic model of bat obstacle avoidance using interaural level differences and distance to the nearest obstacle as the minimal set of cues. In contrast to previous robotic models of bats, the current robot does not attempt to localize obstacles. We evaluate two obstacle avoidance strategies. First, the Fixed Head Strategy keeps the acoustic gaze direction aligned with the direction of flight. Second, the Delayed Linear Adaptive Law (DLAL) Strategy uses acoustic gaze scanning, as observed in hunting bats. Acoustic gaze scanning has been suggested to aid the bat in hunting for prey. Here, we evaluate its adaptive value for obstacle avoidance when obstacles can not be localized. The robot's obstacle avoidance performance is assessed in two environments mimicking (highly cluttered) experimental setups commonly used in behavioral experiments: a rectangular arena containing multiple complex cylindrical reflecting surfaces and a corridor lined with complex reflecting surfaces. The results indicate that distance to the nearest object and interaural level differences allows steering the robot clear of obstacles in environments that return non-localizable echoes. Furthermore, we found that using acoustic gaze scanning reduced performance, suggesting that gaze scanning might not be beneficial under conditions where the animal has limited access to angular information, which is in line with behavioral evidence.

Vampire Bats that Cooperate in the Lab Maintain Their Social Networks in the Wild.

Social bonds, maintained by mutual investments of time and energy, have greatly influenced the evolution of social cognition and cooperation in many species [e.g., 1-8]. However, there are two pitfalls regarding "social bonds" as an explanation for social structure and cooperation [1, 9-11]. First, studies often incorrectly assume that frequent association implies partner fidelity based on mutual social preference, but even seemingly complex nonrandom interaction networks can emerge solely from habitat or spatial structure [12-16]. Second, the false appearance of partner fidelity can result from stable options in the "partner market" [1, 9-11, 17]. For instance, individuals might preferentially groom the same partner, even if the decision depends entirely on the immediate costs and benefits rather than relationship history. Given these issues, a key challenge has been testing the extent to which social structure is driven by the intrinsic relationship history versus the extrinsic physical and social environment. If stable bonds exist, they should persist even if the individuals are moved to a dramatically different physical and social environment. We tested this prediction by tracking social relationships among common vampire bats (Desmodus rotundus) moved from the lab to the wild. We show that allogrooming and food sharing among female vampire bats induced in captivity over 22 months predicted their assortativity and association rates when we subsequently tracked them in the wild with custom-made high-resolution proximity sensors. The persistence of many relationships across different physical and social environments suggests that social structure is caused by both extrinsic constraints and intrinsic partner fidelity.

Maternal mouth-to-mouth feeding behaviour in flower-visiting bats, but no experimental evidence for transmitted dietary preferences.

In addition to breast milk, several mammals feed their offspring with primary food items. This provisioning can offer both energetic and informational benefits: young might use parentally provided food as a source of nutrients, but also as a valuable option to socially learn about adults' food. For bats, there are only very few and partially anecdotal reports of adults feeding their pups with primary food, and there is also a lack of information about social learning processes during ontogeny. In the present study, we provide experimental evidence that lactating flower-visiting bats (Glossophaga soricina) provide regurgitated nectar via mouth-to-mouth feeding behaviour to their pups. After licking at their mothers' slightly opened mouth, pups defecated a marker substance that was exclusively available in the mothers' nectar diet. We additionally investigated associated informational benefits by testing for a social transmission of dietary preferences. We experimentally induced a dietary preference for specifically flavoured nectars to mothers with non-volant pups. Subsequently, after pups became volant, we tested their dietary preferences in a choice experiment. However, we found no experimental evidence that pups adopted the preferences of their mothers.

First cryopreservation of phyllostomid bat sperm.

Bats, the second-largest mammalian order, are widely distributed and provide crucial ecosystem services. Their reproductive biology comprises noteworthy characteristics, such as long-term sperm storage, delayed implantation or even delayed fetal development. The understanding of these mechanisms remains limited. Research in reproductive biology may become crucial for the conservation of endangered bat species. Indeed, the IUCN Red List of Threatened Species currently lists 76 bat species as endangered or critically endangered, for which conservation measures should be taken. The development of assisted reproductive technologies (ART) in bats would thus open new perspectives. In this context we here describe the first successful cryopreservation of bat sperm in the Seba's short-tailed bat (Carollia perspicillata). Epididymal sperm of 30 males was pooled in 6 sample sets and diluted using four different cryo-diluents: Canifreeze, modified Canifreeze, BotuCrio® and Test egg yolk extender. Glycerol and a mixture of glycerol and methylformamide were used as cryoprotectants. Best post-thaw results were achieved when sperm was diluted in Test egg yolk extender containing a mixture of glycerol and methylformamide as cryoprotectant. Post-thaw sperm motility, progressive motility and acrosome integrity of 42.0 ±â€¯3.4%, 28.3 ±â€¯6.3% and 87.7 ±â€¯1.7%, respectively were superior to all other variants tested. It remains to be determined if the post-thaw quality of cryopreserved bat spermatozoa achieved in this study is sufficient for the use in artificial inseminations and produces acceptable pregnancy rates. Successful cryopreservation of spermatozoa in C. perspicillata may serve as the first model to establish gamete rescue programs and develop ART in other, critically endangered bat species.

Presence of humans and domestic cats affects bat behaviour in an urban nursery of greater horseshoe bats (Rhinolophus ferrumequinum).

Proximity to humans is a primary stressor for wildlife, especially in urban habitats where frequent disturbance may occur. Several bat species often roost in buildings but while the effects of disturbance inside the roost are well documented, little is known about those occurring in the proximity of roosts. We tested the effects of anthropogenic stressors on bats by monitoring reactions to disturbance in a colony of greater horseshoe bats (Rhinolophus ferrumequinum). We assessed disturbance by recording and quantifying the presence of people, domestic cats and noise sources near the roost. Disturbance outside the roost caused the disruption of roosting clusters; when cats entered the roost, bats decreased indoor flight activity. Emergence timing was delayed when people were close to the roost exit, and the delay increased along with the number of people. The occurrence of a cat increased the degree of group clustering during emergence. Cats entered the roost especially when young bats were present, and bat remains occurred in 30% of the cat scats we examined. We show that the occurence of human activities near roosts and free-ranging domestic cats are important albeit overlooked sources of disturbance.

Neuroethology of bat navigation.

Once a year about 15 million Mexican free-tailed bats (Tadarida brasiliensis) migrate up to 1,500 kilometers from wintering grounds, seamlessly flying over the Mexican border to enter the United States. Their destination is the Bracken Cave in southern Texas, which will be their summer home between the months of March through October. While residing there, these bats emerge every night at dusk from the narrow 100-foot-wide opening of this enormous cave and begin their nightly commute to foraging grounds located up to 50 kilometers away. Upon arrival, they will spend the night hunting for insects in mid-air while providing a valuable service to local farmers by keeping crop pests in check. Close to the break of dawn, as the night of hunting comes to an end, these bats will begin making their trip back to the roost.

Volitional control of social vocalisations and vocal usage learning in bats.

Bats are gregarious, highly vocal animals that possess a broad repertoire of social vocalisations. For in-depth studies of their vocal behaviours, including vocal flexibility and vocal learning, it is necessary to gather repeatable evidence from controlled laboratory experiments on isolated individuals. However, such studies are rare for one simple reason: eliciting social calls in isolation and under operant control is challenging and has rarely been achieved. To overcome this limitation, we designed an automated setup that allows conditioning of social vocalisations in a new context and tracks spectro-temporal changes in the recorded calls over time. Using this setup, we were able to reliably evoke social calls from temporarily isolated lesser spear-nosed bats (Phyllostomus discolor). When we adjusted the call criteria that could result in a food reward, bats responded by adjusting temporal and spectral call parameters. This was achieved without the help of an auditory template or social context to direct the bats. Our results demonstrate vocal flexibility and vocal usage learning in bats. Our setup provides a new paradigm that allows the controlled study of the production and learning of social vocalisations in isolated bats, overcoming limitations that have, until now, prevented in-depth studies of these behaviours.

An experimental test of effects of ambient temperature and roost quality on aggregation by little brown bats (Myotis lucifugus).

Environmental factors, such as ambient temperature (Ta) or roost/nest quality, can influence social behaviour of small-bodied endotherms because individuals may aggregate for social thermoregulation when Ta is low or select the warmest possible sites for roosting. Female temperate bats form maternity colonies in spring to communally raise pups and exploit social thermoregulation. They also select roosts with warm microclimates because low roost temperature (Troost) delays juvenile development. We studied captive female little brown bats (Myotis lucifugus) to test the hypothesis that variation in Ta and Troost influence social group size. First, we predicted that female bats would preferentially select artificially heated roosts over unheated roosts. Second, we predicted that, as Ta decreased, group size would increase because bats would rely more heavily on social thermoregulation. Third, we predicted that experimentally increasing Troost (i.e., roost quality) above Ta would result in larger group sizes due to greater aggregation in high quality roosts. We captured 34 females from a maternity colony and housed them in a flight-tent provisioned with four bat boxes. Each box was outfitted with a heating pad and thermostat. Over the course of eight-days we heated each roost box in sequence to near thermoneutral Troost for two days. Bats preferentially selected heated roosts over unheated roosts but, contrary to our prediction, group size decreased when Troost was much greater than Ta (i.e., when the benefits of a warm roost should have been highest). Our results suggest that social thermoregulation and the availability of warm roosts influence aggregation in bats and have implications for the potential of summer habitat protection and enhancement to help bat populations in the face of threats like white-nose syndrome.

Younger vampire bats (Desmodus rotundus) are more likely than adults to explore novel objects.

The effects of age on neophobia and exploration are best described in birds and primates, and broader comparisons require reports from other taxa. Here we present data showing age-dependent exploration in a long-lived social species, the common vampire bat (Desmodus rotundus). A previous study found that vampire bats regurgitated food to partners trapped in a cage. Interestingly, while only a few adult bats visited the trapped bat, in every trial all or most of the eight young males in the colony would visit the trapped bat without feeding it. To test whether this behavioral difference resulted from age class differences in exploration, we compared responses of the bats to a trapped conspecific versus an inanimate novel object. Some adults and young showed interest in trapped conspecifics, but only the young males explored the novel objects. Additional novel object tests in a second captive colony showed that higher rates of novel object exploration were shown by young of both sexes. Our results corroborate past findings from other mammals and birds that age predicts exploration. If age-dependent exploration is indeed adaptive, then the role of age as a predictor of exploration tendency should depend on species-specific life history traits. Finally, because younger vampire bats also appear to have higher exposure to pathogens such as rabies virus, there may be implications for pathogen transmission if younger and more exploratory vampire bats are more likely to feed on novel hosts.

Stereotypy and variability of social calls among clustering female big-footed myotis (Myotis macrodactylus).

Echolocating bats have developed advanced auditory perception systems, predominantly using acoustic signaling to communicate with each other. They can emit a diverse range of social calls in complex behavioral contexts. This study examined the vocal repertoire of five pregnant big-footed myotis bats (Myotis macrodactylus). In the process of clustering, the last individual to return to the colony (LI) emitted social calls that correlated with behavior, as recorded on a PC-based digital recorder. These last individuals could emit 10 simple monosyllabic and 27 complex multisyllabic types of calls, constituting four types of syllables. The social calls were composed of highly stereotyped syllables, hierarchically organized by a common set of syllables. However, intra-specific variation was also found in the number of syllables, syllable order and patterns of syllable repetition across call renditions. Data were obtained to characterize the significant individual differences that existed in the maximum frequency and duration of calls. Time taken to return to the roost was negatively associated with the diversity of social calls. Our findings indicate that variability in social calls may be an effective strategy taken by individuals during reintegration into clusters of female M. macrodactylus.

Specialization of the auditory system for the processing of bio-sonar information in the frequency domain: Mustached bats.

For echolocation, mustached bats emit velocity-sensitive orientation sounds (pulses) containing a constant-frequency component consisting of four harmonics (CF1-4). They show unique behavior called Doppler-shift compensation for Doppler-shifted echoes and hunting behavior for frequency and amplitude modulated echoes from fluttering insects. Their peripheral auditory system is highly specialized for fine frequency analysis of CF2 (∼61.0 kHz) and detecting echo CF2 from fluttering insects. In their central auditory system, lateral inhibition occurring at multiple levels sharpens V-shaped frequency-tuning curves at the periphery and creates sharp spindle-shaped tuning curves and amplitude tuning. The large CF2-tuned area of the auditory cortex systematically represents the frequency and amplitude of CF2 in a frequency-versus-amplitude map. "CF/CF" neurons are tuned to a specific combination of pulse CF1 and Doppler-shifted echo CF2 or 3. They are tuned to specific velocities. CF/CF neurons cluster in the CC ("C" stands for CF) and DIF (dorsal intrafossa) areas of the auditory cortex. The CC area has the velocity map for Doppler imaging. The DIF area is particularly for Dopper imaging of other bats approaching in cruising flight. To optimize the processing of behaviorally relevant sounds, cortico-cortical interactions and corticofugal feedback modulate the frequency tuning of cortical and sub-cortical auditory neurons and cochlear hair cells through a neural net consisting of positive feedback associated with lateral inhibition.

Noise interference with echo delay discrimination in bat biosonar.

Echolocating big brown bats (Eptesicus fuscus) were trained in a two-choice task to discriminate differences in the delay of electronic echoes at 1.7 ms delay (30 cm simulated range). Difference thresholds (∼45 µs) were comparable to previously published results. At selected above-threshold differences (116 and 232 µs delay), performance was measured in the presence of wideband random noise at increasing amplitudes in 10-dB steps to determine the noise level that prevented discrimination. Performance eventually failed, but the bats increased the amplitude and duration of their broadcasts to compensate for increasing noise, which allowed performance to persist at noise levels about 25 dB higher than without compensation. In the 232-µs delay discrimination condition, echo signal-to-noise ratio (2E/N0) was 8-10 dB at the noise level that depressed performance to chance. Predicted echo-delay accuracy using big brown bat signals follows the Cramér-Rao bound for signal-to-noise ratios above 15 dB, but worsens below 15 dB due to side-peak ambiguity. At 2E/N0 = 7-10 dB, predicted Cramér-Rao delay accuracy would be about 1 µs; considering side-peak ambiguity it would be about 200-300 µs. The bats' 232 µs performance reflects the intrusion of side-peak ambiguity into delay accuracy at low signal-to-noise ratios.