Vocal learning by greater spear-nosed bats

Functional Ecology

1. To make adaptive behavioral decisions, animals must acquire and process information from their natural and social environment. Reducing uncertainty regarding the actions and goals of conspecifics is especially important for group living animals. 2. Bats are often highly gregarious and use versatile social vocalizations to mediate social interactions. These social vocalizations encode a substantial amount of ecologically relevant information, such as individual identity, sex, and kin. Decoding this information enables receivers to make informed decisions on resource allocation, mate choice, territorial defense, Accepted Article This article is protected by copyright. All rights reserved. and cooperation. Erroneous decisions on such crucial aspects of bats' social behavior can be costly due to reduced reproductive success or survival. 3. Increasingly complex social interactions require social vocalizations encoding more information which, in turn, could facilitate the evolution of even more complex social interactions. Evidence for the positive correlation of social and vocal complexity is available for several taxa but is currently very limited for bats. 4. We conducted a phylogenetic comparative analysis to link the information content encoded in bats' social vocalizations to the complexity of their social lives, i.e., the level of uncertainty associated with assessing individual identity. We focused on three different vocalization types encoding individual signatures (pup isolation calls, adult contact calls, and male-specific vocalizations). Information content in bit (i.e., the number of binary decisions necessary to discriminate among N individuals) was used as an estimate of vocal complexity; relevant social group size (i.e., the number of conspecifics whose identity a receiver could confuse) was used as an estimate of social complexity. 5. Our phylogenetic comparative analysis detected a positive relationship between the information content of vocalizations and the respective relevant social group size. This relationship suggests a positive feedback loop between social and vocal complexity for bat vocalizations and highlights the importance of vocal information for negotiating fitness-relevant social decisions of bats. 6. In conclusion, our work suggests that social complexity drives vocal complexity in bats. Future studies on other hitherto understudied taxa are necessary to establish a comprehensive theory on the multi-faceted coevolution of sociality and communication in the animal kingdom.

Frontiers in Ecology and Evolution, 2020

Social feedback plays an important role in human language development and in the vocal ontogeny of non-human animals. A special form of vocal feedback in humans, infant-directed speech-or motherese-facilitates language learning and is socially beneficial by increasing attention and arousal in the child. It is characterized by high pitch, expanded intonation contours and slower speech tempo. Furthermore, the vocal timbre (i.e., "color" of voice) of motherese differs from the timbre of adult-directed speech. In animals, pup-directed vocalizations are very common, especially in females. But so far there is hardly any research on whether there is a similar phenomenon as motherese in animal vocalizations. The greater sac-winged bat, Saccopteryx bilineata, is a vocal production learner with a large vocal repertoire that is acquired during ontogeny. We compared acoustic features between female pup-directed and adultdirected vocalizations and demonstrated that they differed in timbre and peak frequency. Furthermore, we described pup-directed vocalizations of adult males. During the ontogenetic period when pups' isolation calls (ICs) (used to solicit maternal care) are converging toward each other to form a group signature, adult males also produce ICs. Pups' ICs are acoustically more similar to those of males from the same social group than to other males. In conclusion, our novel findings indicate that parentoffspring communication in bats is more complex and multifaceted than previously thought, with female pup-directed vocalizations reminiscent of human motherese and male pup-directed vocalizations that may facilitate the transmission of a vocal signature across generations.

In colonial species, recognition of offspring should be under strong selection. For accurate identification to occur, offspring must produce individually distinctive signals and parents must be able to discriminate between signals. Female greater spear-nosed bats roost in stable social groups and use infant vocalizations, termed isolation calls, to locate and identify their young. In this study, we investigated both the production and perception of isolation calls in P. hastatus. First, we measured acoustic features of calls and found that, after controlling for ontogenetic effects, sufficient variation exists between pups for isolation calls to function as individual signatures. Moreover, calls of pups from the same social group were more similar in spectral and spectrotemporal features than were calls of pups from different social groups, indicating that these features are probably heritable. We used psychoacoustic experiments in the laboratory to determine whether adult females could discriminate between calls from pups in the same or different social group. Females discriminated between pups when faced with a template-matching task and their performance was correlated with the salience of spectral and spectrotemporal features. We found no difference in performance when females had to discriminate between pups from the same and different social groups.

Springer eBooks, 2006

Animal Behaviour, 1998

The function of social calls emitted by foraging bats has received little study. Here we use observations of free-ranging greater spear-nosed bats, Phyllostomus hastatus, and field playbacks to determine whether audible, broad-band 'screech' calls attract mates, warn conspecifics or influence access to food. Five lines of evidence suggest that screech calls enable adult females from the same roosting group to fly together from the day roost to feeding sites.

Biology Letters, 2010

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.

Biology Letters, 2006

Echolocating bats are auditory specialists, with exquisite hearing that spans several octaves. In the ultrasonic range, bat audiograms typically show highest sensitivity in the spectral region of their species-specific echolocation calls. Welldeveloped hearing in the audible range has been commonly attributed to a need to detect sounds produced by prey. However, bat pups often emit isolation calls with low-frequency components that facilitate mother-young reunions. In this study, we examine whether low-frequency hearing in bats exhibits correlated evolution with (i) body size; (ii) high-frequency hearing sensitivity or (iii) pup isolation call frequency. Using published audiograms, we found that low-frequency hearing sensitivity is not dependent on body size but is related to high-frequency hearing. After controlling for high-frequency hearing, we found that low-frequency hearing exhibits correlated evolution with isolation call frequency. We infer that detection and discrimination of isolation calls have favoured enhanced lowfrequency hearing because accurate parental investment is critical: bats have low reproductive rates, non-volant altricial young and must often identify their pups within large crèches.

PLOS One, 2012

Background: Bat pups produce individually distinct isolation calls to facilitate maternal recognition. Increasing evidence suggests that, in group-living bat species, adults often use similar calls to maintain contact. We investigated if isolated adults from all three species of the highly cooperative vampire bats (Phyllostomidae: Desmodontinae) would produce vocally distinct contact calls when physically isolated.

Animal Behaviour, 2008

We investigated the acoustical component of the recognition process leading to successful mother-pup reunions in the greater sac-winged bat, Saccopteryx bilineata, using both a statistical approach and playback experiments. Statistical evidence for individual distinctiveness was found in the isolation calls uttered by pups and, to a weaker degree, in the echolocation pulse trains emitted by mothers. In contrast to other bat species, isolation calls of S. bilineata pups were complex and multisyllabic, with most of the vocal signature information encoded in the composite syllables at the end of calls. Playback experiments with free-living bats revealed that mothers were able to discriminate between their own pup and an alien young on the basis of isolation calls alone, which confirms the results of the acoustical analysis on vocal signatures in isolation calls. Pups, on the other hand, indiscriminately vocalized in response to echolocation pulse trains from their own and alien mothers, rendering the mother-pup recognition process unidirectional. The one-sidedness of the vocal recognition process in S. bilineata as well as in other bat species might be explained by a lack of selection pressures that shape mutual vocal parent-offspring recognition in other species of mammals and birds. To our knowledge, this study is the first in which playbacks were used to elicit antiphonal calling behaviour between bat mothers and pups experimentally. We argue that vocal responses to playback stimuli are a more feasible and reliable response measure for conducting mother-pup recognition playbacks in bats than the phonotaxis behaviour used in the past.

Frontiers in Ecology and Evolution, 2019

Bats could be a useful study system for studying the evolution of social communication, as they exhibit a high diversity of social group size and complexity. However, the study of bat social calls has been limited, as they are nocturnal, volant animals that produce predominately ultrasonic vocalizations. Passive acoustic monitoring studies occasionally capture bat in-flight social calls. The information from surrounding echolocation calls can provide information on species identity, activity level, and foraging behavior. We used passive acoustic monitoring in Greensboro, North Carolina, to identify seven types of in-flight social calls from Eptesicus fuscus, Lasiurus borealis, Lasiurus cinereus, Nycticeius humeralis, Perimyotis subflavus, and Tadarida brasiliensis. Eptesicus fuscus, N. humeralis, and T. brasiliensis differed in total social call production, and the proportional use of call types. Shared called types exhibited species-specific signatures, indicating the potential for bats to discern signaler identity. Social call production was positively correlated with bat activity. Social calls were often temporally clustered into independent social calling bouts. The complex and upsweep bouts of E. fuscus were associated with foraging, and the likelihood of complex bouts was negatively correlated with heterospecific activity. The production of N. humeralis downsweep, downsweep-upsweep, and upsweep bouts varied by season and site, but not according to bat activity, foraging, or time of night. Species differed in which call types were most commonly emitted, and these calls are associated with different contexts, suggesting that bats exhibit species-specific differences in in-flight social behavior.

2020

Behavioral Ecology and Sociobiology, 2011

In several bird and mammal species, contact calls are utilized to maintain group cohesion and coordinate group movement. From a signal design perspective, contact calls typically exhibit acoustic features that make them easily localizable and encode information about individual or group identity. Pallid bats (Antrozous pallidus) are unusual among vespertilionids in that they often emit a loud, partially audible frequency-modulated social call several times in rapid succession while in flight. This call appears to function as a contact call in that it is frequently given when bats return from foraging and perform circular flights before entering a crevice roost. However, the degree to which pallid bats respond to the calls of conspecifics and what information is provided in the call is unknown. Thus, the goal of this study was to investigate pallid bat calling behavior to determine if calls attract roostmates or elicit responses from them and provide sufficient information for individual recognition. In playback studies, we found that contact calls elicit calls and approaches and that free-flying bats respond more to familiar than unfamiliar calls. In addition, analysis of frequency and temporal measurements of calls collected from multiple sites and spectral cross correlation analysis of calls recorded from the same radiotagged bats on multiple evenings revealed that the frequency pattern of contact calls is highly repeatable over time within individuals but exhibits significant differences among individuals. Thus, contact call structure appears to be unique to individuals and stable through time, which makes these calls well-suited for roostmate recognition. Keywords Communication. Signature call. Fission-fusion. Vespertilionid bat Benefits of group living in animals include predator detection, information transfer about foraging sites, and social thermoregulation (Krebs and Davies 1993). To obtain these benefits, a mechanism to maintain group cohesion is necessary, especially when individuals in the group are highly mobile. One such mechanism utilized by several bird and mammal species is the use of a specialized vocal signal, typically designated as a contact call. From a signal design perspective, contact calls are often high in amplitude and easily localizable, with the broadcast range of the call often closely tied to the dispersion of the group. In addition, variation in frequency modulation, temporal pattern, and harmonic structure can encode information about the individual or the social composition of its group (Bradbury and Vehrencamp 1998). For example, northern resident killer whales (Orcinus orca) live in stable family groups and produce contact calls that are specific to groups, and to a lesser extent, individuals (Nousek et al. 2006). Alternatively, in more fluid societies, there is little benefit to maintain group signatures due to the frequent immigration and emigration of individuals. Thus, contact calls often encode individual signatures, which may aid in maintaining non-random associations among group members (Cortopassi and Bradbury 2006). For example, fission-fusion social structure is characteristic of many avian and mammalian societies where subgroups are part of a larger group that frequently splits or merges together (Couzin 2006), and many species with this type of social system produce individually specific contact calls [e.g., spider monkeys, Ateles geoffroyi (Ramos-Fernandez 2005); orange-fronted parakeets, Aratinga canicularis (Cortopassi and Bradbury Communicated by G. Jones

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 amongindividual 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'. Group-living animals often use acoustic signals to coordinate costly, risky or challenging collective behaviours, such as group hunting [1-3], formation

Behavioral Ecology

Animals have evolved diverse strategies to use social information for increasing foraging success and efficiency. Echolocating bats, for example, can eavesdrop on bats foraging nearby because they shift from search-phase calls to feeding buzzes when they detect prey. Feeding buzzes can directly convey information about prey presence, but it is unknown whether search-phase calls also convey social information. Here, we investigated whether search-phase echolocation calls, distinct calls produced by some bat species to scan large open areas for prey, can additionally convey individual identity. We tested this in Molossus molossus, a neotropical insectivorous bat that forages with group members, presumably to find ephemeral insect swarms more efficiently. We caught M. molossus from six different social groups and recorded their search-phase calls during a standardized release procedure, then recaptured and tested 19 marked bats with habituation–dishabituation playback experiments. We s...