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.Publisher PDFPeer reviewe

Pup Directed Vocalizations of Adult Females and Males in a Vocal Learning Bat

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 adult-directed 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 parent-offspring 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

Thermoregulatory Requirements Shape Mating Opportunities of Male Proboscis Bats

The spatiotemporal distribution of females is a major factor affecting animal social systems. Predation risk and the distribution of feeding resources often determine where females are found, but abiotic factors (e.g., temperature) can also shape the distribution of females and therefore variation in social organization and mating systems. Given the predicted future changes in climatic variation, it is vital to understand how animal mating systems and the sexual selection process may be altered by temperature. In bats, female distribution is tightly linked to roosting ecology and particularly to the microclimatic conditions at the roost. Proboscis bats (Rhynchonycteris naso) form cohesive and stable multi-male-multi-female groups and inhabit exposed day roosts (e.g., tree trunks, vines, buildings). Strong selection to remain inconspicuous to visually oriented predators in the exposed day roosts has been suggested to promote a rather rare male mating strategy termed site-specific dominance where males defend females directly but are successful in doing so only in their own territory. The choice of open-roost structures can result in the bats roosting under direct sunlight, making individuals susceptible to overheating. Here we investigate whether regular relocations of R. naso social groups among male territories are a mechanism of behavioral thermoregulation. Our results suggest that in general R. naso choose the warmest suitable roost sites within a roost, possibly to minimize the energetic costs of thermoregulation. However, on days with high midday temperatures at the primary roost site, bats commonly relocate to alternative, cooler sites within their roosts. These thermoregulatory relocations entail that a social group regularly switches among the territories of several males. Thus, the need for behavioral thermoregulation determines the spatial distribution of females and shapes the mating opportunities of males during the day. This is supported by our result that territorial males defending primary roost sites are reproductively more successful than territorial males of alternate roost sites. In line with other studies, our findings suggest that the increase in ambient temperatures associated with climate change has the potential to affect the intensity of sexual selection in bat species and may have far-reaching behavioral, demographic, and evolutionary consequences for their populations

Isolation calls of the bat saccopteryx bilineata encode multiple messages

The information that can possibly be encoded in a given vocalization is limited by the available acoustic space. Vocalizations composed of several elements have the potential to distribute information among distinct elements and thus encode various layers of information simultaneously. Correspondingly, the multiple messages hypothesis states that different elements of a vocalization convey different information, for example, about identity, signallers’ quality or external events, which is directed to one or several receivers. The isolation call of the greater sac-winged bat, Saccopteryx bilineata, is a complex vocalization composed of different syllable types (variable, composite and stereotyped syllables). Pups produce isolation calls to elicit maternal care. In contrast to most bats, isolation calls of S. bilineata remain part of the adult vocal repertoire. In this study, we investigated the acoustic trajectories of isolation calls during ontogeny. Our analyses demonstrated that ontogenetic changes of acoustic parameters were most pronounced in stereotyped syllables. Throughout ontogeny, stereotyped syllables became shorter in duration and higher in frequency and bandwidth, thus effectively encoding information about age. Additionally, former studies revealed that composite syllables encode both an individual and a group signature. In our study, we also found an individual signature, thus corroborating the previous study. We conclude that isolation calls of S. bilineata encode multiple messages which are temporally segregated. The composite syllables conveyed information about individual identity and social group affiliation, whereas the stereotyped syllables encoded information about age. The temporal segregation allows the separation of information conveyed by distinct elements, thus enhancing signal reliability

Territorial choruses of giant otter groups (Pteronura brasiliensis) encode information on group identity

Group living animals often engage in corporate territorial defence. Territorial group vocalizations can provide information about group identity, size and composition. Neighbouring groups may use this information to avoid unfavourable direct conflicts. Giant otters are highly social and territorial animals with an elaborate vocal repertoire. They produce long-range screams when they are alert or excited, i.e. in an alarm, isolation or begging context. Long-range screams are not only produced by one individual at a time (‘single screams’) but also by multiple group members simultaneously, resulting in a highly conspicuous ‘group chorus’. Wild giant otters regularly produce group choruses during interactions with predators, when they detect intruders in their territory or before group reunions after separation. Since single screams and especially group choruses probably contribute to the groups’ corporate territorial defence, we hypothesized that group identity is encoded in single screams and group choruses. We analysed vocalizations from five wild and three captive giant otter groups and found statistical evidence for a group signature in group choruses. Results for single screams were less conclusive, which might have been caused by the comparatively lower sample size. We suggest that giant otters may gain information on group identity by listening to group choruses. Group identity likely constitutes important social information for giant otters since territory boundaries of neighbouring groups can overlap and direct inter-group conflicts are severe. Therefore, group chorusing may contribute to the mutual avoidance of members from different groups

Structurally rich dry grasslands – Potential stepping stones for bats in open farmland

Agricultural intensification has caused decrease and fragmentation of European semi-natural dry grasslands. While a high biodiversity value of dry grasslands is acknowledged for plants and insects, locally and on landscape level, their relevance for mobile species, such as bats, is unknown. Here we investigate the use of dry grassland fragments by bats in an agriculturally intensified region in Germany and evaluate local and landscape factors influencing bat activity and assemblages. Specifically, we predicted that a combination of local dry grassland structural richness and landscape features as well as their interactions affect bat activity and foraging above dry grasslands. We also expected that these features influence compositions of local bat assemblages. We repeatedly sampled at 12 dry grassland plots with acoustic monitoring and assessed activity and foraging of bat species/sonotypes, which we grouped into guilds known for foraging in open land, at vegetation edges and in narrow spaces. We determined structural richness of the dry grassland plots in field and derived landscape features from digital landscape data. A relatively high proportion of bat species/sonotypes used dry grasslands regularly. The edge space foragers responded positively to higher local structural richness. Their dry grassland use increased when surrounding forests and woody features were less available, but they foraged more on dry grasslands closer to water bodies. Narrow space bat activity on dry grasslands decreased with less landscape connectivity. Open and narrow space foragers responded to local structural richness only in landscape context. For all bat guilds we found increased use of structurally richer dry grasslands when there was more open farmland in the surroundings. This was also the case for edge space foragers, when landscapes were more homogeneous. Lastly, with increasing structural richness, bat assemblages were more dominated by edge space foragers. We show the importance of European dry grassland fragments for the highly mobile group of bats under certain local structural and landscape compositional conditions. Our results underline the value of heterogeneous dry grassland fragments as potential stepping stones in intensively used farmland areas and contribute to evidence based decision making in dry grassland management and bat conservation

Structurally rich dry grasslands – Potential stepping stones for bats in open farmland

Agricultural intensification has caused decrease and fragmentation of European semi-natural dry grasslands. While a high biodiversity value of dry grasslands is acknowledged for plants and insects, locally and on landscape level, their relevance for mobile species, such as bats, is unknown. Here we investigate the use of dry grassland fragments by bats in an agriculturally intensified region in Germany and evaluate local and landscape factors influencing bat activity and assemblages. Specifically, we predicted that a combination of local dry grassland structural richness and landscape features as well as their interactions affect bat activity and foraging above dry grasslands. We also expected that these features influence compositions of local bat assemblages. We repeatedly sampled at 12 dry grassland plots with acoustic monitoring and assessed activity and foraging of bat species/sonotypes, which we grouped into guilds known for foraging in open land, at vegetation edges and in narrow spaces. We determined structural richness of the dry grassland plots in field and derived landscape features from digital landscape data. A relatively high proportion of bat species/sonotypes used dry grasslands regularly. The edge space foragers responded positively to higher local structural richness. Their dry grassland use increased when surrounding forests and woody features were less available, but they foraged more on dry grasslands closer to water bodies. Narrow space bat activity on dry grasslands decreased with less landscape connectivity. Open and narrow space foragers responded to local structural richness only in landscape context. For all bat guilds we found increased use of structurally richer dry grasslands when there was more open farmland in the surroundings. This was also the case for edge space foragers, when landscapes were more homogeneous. Lastly, with increasing structural richness, bat assemblages were more dominated by edge space foragers. We show the importance of European dry grassland fragments for the highly mobile group of bats under certain local structural and landscape compositional conditions. Our results underline the value of heterogeneous dry grassland fragments as potential stepping stones in intensively used farmland areas and contribute to evidence based decision making in dry grassland management and bat conservation

Similarities in social calls during autumn swarming may facilitate interspecific communication between Myotis bat species

Bats employ a variety of social calls for communication purposes. However, for most species, social calls are far less studied than echolocation calls and their specific function often remains unclear. We investigated the function of in-flight social calls during autumn swarming in front of a large hibernaculum in Northern Germany, whose main inhabitants are two species of Myotis bats, Natterer’s bats (Myotis nattereri) and Daubenton’s bats (Myotis daubentonii). We recorded social calls in nights of high swarming activity and grouped the calls based on their spectro-temporal structure into ten types and verified our visual classification by a discriminant function analysis. Whenever possible, we subsequently assigned social calls to either M. daubentonii or M. nattereri by analyzing the echolocation calls surrounding them. As many bats echolocate at the same time during swarming, we did not analyze single echolocation calls but the “soundscape” surrounding each social call instead, encompassing not only spectral parameters but also the timbre (vocal “color”) of echolocation calls. Both species employ comparatively similar social call types in a swarming context, even though there are subtle differences in call parameters between species. To additionally gain information about the general function of social calls produced in a swarming context, we performed playback experiments with free-flying bats in the vicinity of the roost, using three different call types from both species, respectively. In three out of six treatments, bat activity (approximated as echolocation call rate) increased during and after stimulus presentation, indicating that bats inspected or approached the playback site. Using a camera trap, we were sometimes able to identify the species of approaching bats. Based on the photos taken during playbacks, we assume one call type to support interspecific communication while another call type works for intraspecific group cohesion

the impact of roosting ecology on a bat's mating strategy

With their extraordinary species richness and diversity in ecological traits and social systems, bats are a promising taxon for testing socio-ecological hypotheses in order to get new insights into the evolution of animal social systems. Regarding its roosting habits, proboscis bats form an extreme by occupying sites which are usually completely exposed to daylight (e.g. tree trunks, vines or rocks). This is accompanied by morphological and behavioural adaptations to remain cryptic in exposed day roosts. With long-term behavioural observations and genetic parentage analyses of individually marked proboscis bats, we assessed its social dispersion and male mating strategy during day and night. Our results reveal nocturnal male territoriality—a strategy which most closely resembles a resource-defence polygyny that is frequent also in other tropical bats. Its contrasting clumped social dispersion during the day is likely to be the result of strong selection for crypsis in exposed roosts and is accompanied by direct female defence in addition to male territoriality. To the best of our knowledge, such contrasting male mating strategies within a single day–night cycle have not been described in a vertebrate species so far and illustrate a possible evolutionary trajectory from resource-defence to female-defence strategy by small ecologically driven evolutionary steps

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