Elsevier

Current Opinion in Neurobiology

Volume 28, October 2014, Pages 80-85
Current Opinion in Neurobiology

Vocal production learning in bats

https://doi.org/10.1016/j.conb.2014.06.014Get rights and content

Highlights

  • Bat echolocation is a preadaptation for sophisticated vocal communication.

  • Thus, bats are a highly promising taxon for studies on vocal production learning.

  • There is evidence for respiratory and phonatory learning but not for filter learning.

  • Comparative studies on mammalian vocal production learning are especially rewarding.

  • The taxon's speciose nature makes phylogenetically controlled studies possible.

Echolocating bats exhibit excellent control over their acoustic signals emitted and skillfully interpret the returning echoes, allowing orientation and foraging in complete darkness. Echolocation may be a preadaptation for sophisticated vocal communication with conspecifics and, ultimately, vocal learning processes. In humans, the importance of auditory input for correct speech acquisition is obvious, whereas vocal production learning is rare and patchily distributed among non-human mammals. Bats comprise one of the few mammalian taxa capable of vocal production learning, with current behavioral evidence for three species belonging to two families; more evidence will probably forthcoming. The taxon's speciose nature makes bats well suited for phylogenetically controlled, comparative studies on proximate and ultimate mechanisms of mammalian vocal production learning.

Introduction

While many taxa show the ability to learn the usage and comprehension of acoustic signals, only a select few are capable of vocal production learning (reviewed in [1, 2, 3]). Vocal production learning requires both excellent control over the sound production apparatus and a neural interface that coordinates precise adjustments in signal production according to the auditory input received. Two general types of vocal production learning exist, namely social modification and learned acquisition (sensu [3]). Social modification refers to gradual changes of already existing signals, whereas learned acquisition denotes the acquirement of new signals. Both learning types rely on vocal influences from conspecifics; however, each type may be subjected to different selective pressures and require different behavioral and neural mechanisms.

Bats are a promising taxon to study vocal production learning because their highly flexible echolocation behavior requires remarkable control during signal production and rapid, precise auditory perception when interpreting the returning echoes (reviewed in e.g. [4, 5, 6, 7]). Moreover, many bat species are both very gregarious and long-lived [8, 9], providing ample opportunities to learn from conspecifics [10, 11]. Despite these widespread prerequisites, current evidence for vocal production learning in bats remains scarce. This discrepancy is most likely caused by the difficulty of studying these nocturnal, highly mobile animals. The following section provides a short overview of current knowledge on vocal production learning in bats. Afterwards, I discuss proximate and ultimate mechanisms and highlight promising avenues of future research.

Section snippets

Case studies

To date, three bat species from two families are known to be capable of vocal production learning. However, it is likely that more vocal learning bat species exist, because only a fraction of the speciose taxon has been investigated so far. Vocal production learning can shape social vocalizations of both sexes [12••, 13••, 14••, 15••], while evidence for its influence on echolocation calls is feasible but less certain (see [16•, 17]). Learned bat vocalizations may be shaped by natural selection

Pale spear-nosed bats, Phyllostomus discolor (Phyllostomidae)

Both observational and experimental studies on captive pale spear-nosed bats, a tropical New World species, demonstrate convincingly that pups progressively adapt their isolation calls to maternal directive calls ([18]; Figure 1a) or to an invariable computer-generated directive call which was broadcast to pups that were hand-reared in isolation [12••]. Pup isolation calls and maternal directive calls are sinusoidally frequency-modulated signals which are produced antiphonally during

Greater spear-nosed bats, Phyllostomus hastatus (Phyllostomidae)

An experimental study on captive greater spear-nosed bats, another tropical New World species, provided unequivocal evidence that a vocalization type facilitating group foraging encodes a group signature that is maintained by vocal production learning [13••]. Phyllostomus hastatus forms stable groups of unrelated females which communicate via noisy screech calls during joint foraging bouts [21]. Screech calls of different individuals are statistically indistinguishable, whereas considerable

Greater sac-winged bats, Saccopteryx bilineata (Emballonuridae)

Several observational studies demonstrate conclusively that both social modification and learned acquisition exist in the tropical New World bat Saccopteryx bilineata. Pup isolation calls are innate signals encoding an individual signature that is used by mothers to discriminate between their own and alien pups [24]. These isolation calls also encode a group signature that is modified over time based on vocal influences of other pups belonging to the same social group ([15••]; Figure 1c).

Proximate mechanisms

The vocal production apparatus consists of different components, namely respiratory, phonatory and filter systems (reviewed in [31]), all of which could be influenced by learning processes. Changing frequency characteristics is considered to be more difficult than changing temporal characteristics [2, 3]. In bats, there is evidence for respiratory and phonatory learning (Figure 1a–d), but no evidence for vocal tract filter learning so far. Chiropteran filter learning constitutes an interesting

Ultimate mechanisms

Assuming that it is beneficial for the signaler to be recognized, vocal production learning is adaptive when signal similarity is essential for signal function and cannot be encoded genetically, e.g. when signals indicate group membership among unrelated individuals (as in the bat P. hastatus; [13••]), or when signal similarity enhances signal function in addition to a genetic encoding, e.g. when pup isolation calls converge towards their mothers’ calls (as in the bat P. discolor; [12••]). The

Conclusions

Bats are highly promising candidates for in-depth studies on mammalian vocal production learning. The speciose nature of this taxon (more than 1100 extant species; [46]) allows for comparative studies on selective pressures shaping the occurrence of vocal production learning while controlling for phylogenetic effects. In addition to the two families already known to contain vocal learning species (Phyllostomidae, Emballonuridae), four other families are of special interest for future studies,

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Conflict of interest

Nothing declared.

Acknowledgements

I am indebted to the German Baden-Württemberg Stiftung, Eliteprogramme for Postdocs, for the financial support of my research. In addition, I thank M. Metz, M. Nagy, H.-U. Schnitzler and G. Jones for fruitful discussions, and T. Fitch for critical comments on the manuscript.

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