Kirsten M. Bohn

Syllable acoustics, temporal patterns, and call composition vary with behavioral context in Mexican free-tailed bats

Recent research has shown that some bat species have rich vocal repertoires with diverse syllable acoustics. Few studies, however, have compared vocalizations across different behavioral contexts or examined the temporal emission patterns of vocalizations. In this paper, a comprehensive examination of the vocal repertoire of Mexican free-tailed bats, T. brasiliensis, is presented. Syllable acoustics and temporal emission patterns for 16 types of vocalizations including courtship song revealed three main findings. First, although in some cases syllables are unique to specific calls, other syllables are shared among different calls. Second, entire calls associated with one behavior can be embedded into more complex vocalizations used in entirely different behavioral contexts. Third, when different calls are composed of similar syllables, distinctive temporal emission patterns may facilitate call recognition. These results indicate that syllable acoustics alone do not likely provide enough information for call recognition; rather, the acoustic context and temporal emission patterns of vocalizations may affect meaning.

Versatility and Stereotypy of Free-Tailed Bat Songs

In mammals, complex songs are uncommon and few studies have examined song composition or the order of elements in songs, particularly with respect to regional and individual variation. In this study we examine how syllables and phrases are ordered and combined, ie “syntax”, of the song of Tadarida brasiliensis, the Brazilian free-tailed bat. Specifically, we test whether phrase and song composition differ among individuals and between two regions, we determine variability across renditions within individuals, and test whether phrases are randomly ordered and combined. We report three major findings. First, song phrases were highly stereotyped across two regions, so much so that some songs from the two colonies were almost indistinguishable. All males produced songs with the same four types of syllables and the same three types of phrases. Second, we found that although song construction was similar across regions, the number of syllables within phrases, and the number and order of phrases in songs varied greatly within and among individuals. Last, we determined that phrase order, although diverse, deviated from random models. We found broad scale phrase-order rules and certain higher order combinations that were highly preferred. We conclude that free-tailed bat songs are composed of highly stereotyped phrases hierarchically organized by a common set of syntactical rules. However, within global species-specific patterns, songs male free-tailed bats dynamically vary syllable number, phrase order, and phrase repetitions across song renditions.

Discrimination of Infant Isolation Calls by Female Greater Spear-Nosed Bats, Phyllostomus hastatus.

In colonial species, recognition of offspring should be under strong selection. For accurate identification to occur offspring must emit individually distinctive signals and parents must be able to discriminate between signals. Female greater spear-nosed bats (Phyllostomus hastatus) roost in stable social groups and use infant vocalizations, termed isolation calls, to locate and identify their young. In this study, we investigate both the production and perception of isolation calls in P. hastatus. First, we measured acoustic features and found that after controlling for ontogenetic effects, sufficient variation exists between pups for isolation calls to function as individual signatures. Moreover, pups from the same social group emit calls with more similar spectral and spectro-temporal features than pups from different social groups, indicating that these features are likely heritable. We used psychoacoustic experiments in the laboratory to determine if 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 spectro-temporal features. We found no difference in performance when females had to discriminate between pups from the same and different social groups. These results indicate that females should be able to accurately identify their young using isolation calls.

Social context evokes rapid changes in bat song syntax

The capacity to modify vocal syntax to changes in social context is an important component of vocal plasticity and complexity in adult vertebrates, especially in human speech. The ecological significance of this behaviour has been well established in some avian species but not in mammals where complex, multisyllabic vocalizations are rare. The Brazilian free-tailed bat, Tadarida brasiliensis, is a mammal that sings like a bird, producing hierarchically structured songs that vary in the order and number of phrases (i.e. syntax) from one rendition to the next while simultaneously following specific organizational rules. Here, we used playback experiments to examine the function of songs and tested whether song syntax is correlated with social context. Free-tailed bats responded rapidly and robustly to echolocation calls that mimicked a bat flying past the roost but did not respond to conspecific song playbacks. We compared songs that were directed at a passing bat with songs that were produced spontaneously and found that bats produced longer songs with different phrase content and order when singing spontaneously than when singing to bats approaching their roost. Thus, free-tailed bats quickly varied song composition to meet the specific demands of different social functions. These distinct singing behaviours are similar to those of some songbirds, suggesting that bats and birds have converged upon a similar set of production modes that may reflect common neural mechanisms and ecological factors.

Pup guarding by greater spear-nosed bats

Alloparental care poses an evolutionary dilemma because effort is expended on non-filial offspring. Thus, instances of alloparental care have been attributed to either mistaken identity, (i.e., recognition errors) or active cooperation. In greater spear-nosed bats (Phyllostomus hastatus), reproductive females roost together in stable long-term social groups in cave ceilings. Non-volant pups frequently fall from roost sites to the cave floor where they can die unless retrieved by an adult. In this study, we examined the function of adult female visits to non-filial young and tested whether visits were attributable to recognition errors or to cooperation. We found that females visited non-filial pups from their own social group more than expected. Females from different social groups attacked and sometimes killed pups, and male pups were attacked more frequently than female pups. Visits by group mates benefited fallen pups by reducing the likelihood of attack by females from other groups. In contrast to the mistaken identity hypothesis, we found that some females leave their own pups to approach and remain with group mates’ pups. We used microsatellite markers to estimate relatedness and test whether kinship could explain this alloparental care and found that females were unrelated to the pups they guard. We conclude that females who reside in highly stable social groups exhibit cooperative behavior that cannot be explained by kinship and is unlikely to be due to direct or generalized reciprocity. Instead, our data suggest that alloparental care likely involves a complex interplay between group membership and cooperative foraging.

Correlated evolution between hearing sensitivity and social calls in bats

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. Well-developed 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 low-frequency 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.

Non-kin cooperation in bats.

Many bats are extremely social. In some cases, individuals remain together for years or even decades and engage in mutually beneficial behaviours among non-related individuals. Here, we summarize ways in which unrelated bats cooperate while roosting, foraging, feeding or caring for offspring. For each situation, we ask if cooperation involves an investment, and if so, what mechanisms might ensure a return. While some cooperative outcomes are likely a by-product of selfish behaviour as they are in many other vertebrates, we explain how cooperative investments can occur in several situations and are particularly evident in food sharing among common vampire bats (Desmodus rotundus) and alloparental care by greater spear-nosed bats (Phyllostomus hastatus). Fieldwork and experiments on vampire bats indicate that sharing blood with non-kin expands the number of possible donors beyond kin and promotes reciprocal help by strengthening long-term social bonds. Similarly, more than 25 years of recapture data and field observations of greater spear-nosed bats reveal multiple cooperative investments occurring within stable groups of non-kin. These studies illustrate how bats can serve as models for understanding how cooperation is regulated in social vertebrates.

Audio-vocal feedback in bats and new roles for echolocation calls in social communication

An important aspect of auditory scene analysis is the specialized neurocircuitry required for vocal production. in a dynamic acoustic environment. Although often taken for granted, enhanced audio-vocal feedback is relatively uncommon in animals and yet an important precursor to vocal learning. We argue that vocal complexity in bats is an exaptation of the highly specialized audio-vocal feedback system that has evolved for echolocation. First, we explore how audio-vocal feedback enhances echolocation. Second, we review how echolocation pulses serve social functions by providing information to receivers (like gender, identity, or food availability). Third, using our research on molossid bats (family Molossidae), we explore whether vocal plasticity in sonar has contributed to an expanded role for sonar pulses in social communication. In at least three molossids, roosting bats rapidly sing in response to echolocation pulses of flying conspecifics. However, more importantly, we show that in multiple species, echolocation is produced in purely social contexts. Roosting bats embed pulses and feeding buzzes into their courtship songs that are not acoustically distinct than when foraging. Finally, some molossids not only sing in roosts, but also in flight—that is, they echolocate and sing simultaneously. These findings indicate that echolocation plays even more of a role in social communication than commonly believed and that the production of echolocation and social communication is tightly coupled and coordinated at a high level.

The Complex Songs of Two Molossid Species

Birds are well known for songs while bats are well known for their developed sonar system. The chiropteran echolocation system has a long and extensive history of research because of the highly specialized neurocircuitry required for vocal production, perception, and vocal-motor integration. However, recent research has revealed that in addition to echolocation, bats produce highly sophisticated social vocalizations whose complexity is only rivaled by birds, humans, and cetaceans. In this chapter we discuss and define the terms “song” and “courtship call”, outline how acoustic signals are analyzed, and review what families of bats produce songs and calls. We then compare behavior, song structure, individual variation, and regional dialects in two species of Molossids, Tadarida brasiliensis and Nyctinomops laticaudatus. T. brasiliensis is a bat that sings like a bird—they produce songs with three key songbird features: hierarchical structure, syntactical organization, and syntactical flexibility. T. brasiliensis songs are composed of four main syllable types: chirp A (“A”), chirp B (“B”), trill and buzz. Syllables are combined to form three phrases, chirp, trill, and buzz and phrases are then combined to form songs (hierarchical structure). Specific syntactical rules are followed for combining phrases (syntactical organization). However, the number of syllables within a phrase and the number and order of phrases vary from one rendition to the next (syntactical flexibility). N. laticaudatus produce the same types of syllables and phrases as T. brasiliensis. However, the spectro-temporal structure of A and B syllables of N. laticaudatus are quite different, and they show much lower syntactical flexibility in combining phrases. Finally, while T. brasiliensis males produce highly stereotyped chirp syllables that do not vary between regions, N. laticaudatus chirp syllables are not stereotyped within males but do vary across regions. These findings are the first to show that complex songs are not only produced by a single bat species and that many aspects of songs are highly conserved across species.

Bats as new models for social communication

Bat echolocation has been the focus of extensive acoustic research for over 50 years. However, our knowledge of bat social communication is in its infancy, having really only begun to develop over the last decade. This is because only recently have ultrasonic recording and playback become affordable, rugged, and portable—making field research highly expedient. These advances have in essence opened up an entirely new frontier in acoustic research. Indeed a very large frontier with over 1000 diverse species, nearly all of which are highly social. Here, I review the types of vocalizations bats produce, from echolocation calls, to simple calls to complex songs. For example, simple infant isolation calls are produced by the majority of mammals with little to no specialization in bats. In contrast, our work on Molossid bats shows that they embed “echolocation” calls into complex song phrases while roosting and in flight. In this case, social communication is likely an exaptation of the highly specialized echolocation system. Finally, I discuss where bats fit into our current models—birds, anurans, cetaceans, and rodents—and how using a comparative approach can greatly expand our understanding of acoustic communication.