Babbling in a vocal learning bat resembles human infant babbling

Babbling bats A notable aspect of language development in humans is the babbling stage. During this time, toddlers make a range of specific sounds as they practice and imitate adult speech. Humans are not the only vocal learners, however, so might we expect such babbling among others? Fernandez et al. recorded the vocalizations of sac-winged bat pups in the wild and found clear evidence of babbling that was consistent with that seen in humans. The shared babbling components suggest that vocal learning may have similar specific mechanisms across a wide array of mammalian species. Science, abf9279, this issue p. 923 Young Saccopteryx bilineata bat pups babble as they learn to vocalize, with similar features to those that define babbling in human infants. Babbling is a production milestone in infant speech development. Evidence for babbling in nonhuman mammals is scarce, which has prevented cross-species comparisons. In this study, we investigated the conspicuous babbling behavior of Saccopteryx bilineata, a bat capable of vocal production learning. We analyzed the babbling of 20 bat pups in the field during their 3-month ontogeny and compared its features to those that characterize babbling in human infants. Our findings demonstrate that babbling in bat pups is characterized by the same eight features as babbling in human infants, including the conspicuous features reduplication and rhythmicity. These parallels in vocal ontogeny between two mammalian species offer future possibilities for comparison of cognitive and neuromolecular mechanisms and adaptive functions of babbling in bats and humans.

K ey components of spoken language include the ability to modify a signal on the basis of auditory input [called vocal production learning (1)], syntactical composition, and semantic reference (2). Speech, the vocal motor output of language, requires precise control over the articulators of the vocal apparatus. The first utterances resembling speech sounds occur during babbling, a distinctive vocal behavior of human infants (3,4). The ability to produce canonical syllables, such as "da'da," during babbling is required for successful language acquisition, and age-appropriate babbling is an indication of typical child development (4). Babbling enables infants to practice speech sounds by gaining control over the speech articulators and probably by reinforcing neuromotor connections (4). This behavior is characterized by universal features (Table 1).
Evidence for babbling exists in very few nonhuman taxa (table S1), one of which is the greater sac-winged bat (Saccopteryx bilineata). This neotropical bat exhibits vocal production learning (5) in addition to a conspicuous vocal practice behavior during ontogeny (figs. S1 and S2). This vocal practice has been described as resembling human infant babbling (6), but formal analyses have been lacking. The auditory input of S. bilineata pups consists of various conspecific vocalizations, the most notable being multisyllabic songs that adult males produce daily to defend their territories and attract females (figs. S3 and S4) (7). During babbling, pups acquire territorial songs by imitating adult tutors (5,6). In this Report, we provide the first formal comparison of babbling features across mammals capable of vocal production learning and show that babbling behavior in S. bilineata pups is characterized by features similar to those of babbling in human infants.
We investigated the undisturbed, unmanipulated babbling behavior of 20 pups from two wild populations in Costa Rica and Panama throughout the pups' vocal ontogeny and analyzed 55,056 syllables from 216 babbling bouts ( Fig. 1) (8). We defined a syllable as a sound surrounded by silence; the term is thus not synonymous to the speechlike syllables produced by human infants (Table 1). For 7 to 10 weeks, pups spent almost 30% of their diurnal activity with vocal practice (fig. S2B). Babbling bouts were composed of several multisyllable trains ( fig. S5) and had an average duration of 7 min; a single bout could last up to 43 min [adult vocalizations have a duration of several seconds to less than 1 min (7)].
Pup babbling started within the first 3 weeks after birth, at approximately one-third of the way through their 10-week vocal ontogeny ( Fig. 2A). The adult vocal repertoire of S. bilineata consists of 25 different syllable types that are combined in various ways into 10 distinct vocalization types (7,9). Producing the different syllable types during a pronounced babbling phase might be necessary to gain precise control over the vocal apparatus by means of sensorimotor learning. Pup babbling occurs during a circumscribed early developmental period and likely reflects a sensitive period for vocal production learning, as has been documented in humans and songbirds (10).

Feature Description
Early babbling onset Marginal babbling occurs from~3 months onward; canonical babbling occurs from~6 to 7 months onward; variegated babbling normally begins later than canonical babbling (3)

Syllable subset acquisition
Production of a small, universal subset of all syllable types that occur in natural languages (4) . were exclusively present during the entire babbling phase, clearly distinguishable from the adultlike syllable types (table S2), and not part of the adult vocal repertoire. These protosyllables were the most frequent syllable type in babbling bouts (39% of syllables; data S1) and were highly variable (table S3). This high variability may reflect vocal exploration and may help pups to shape their vocal output toward adult vocalizations in an apparently playful manner. Furthermore, undifferentiated protosyllables might facilitate the production switch between two distinct adultlike syllable types, because undifferentiated protosyllables were mainly located between them ( fig. S6). Fernandez (3)], followed by a period during which previously unused syllable types emerged only infrequently and unequally across pups (Fig. 2D). Babbling bouts were dominated by the reduplication of syllable types (Fig. 2E): 77% of syllables were succeeded by those belonging to the same syllable type, and the observed reduplication rate was significantly higher than the predicted reduplication rate based on the number of produced syllables (data S1). Similar to vocal learning behaviors in human infants, the benefit of syllable reduplication in bat pups may be to support vocal practice by repetition ("rehearsing"), likely by facilitating neural sensorimotor integration (11). In humans, one proximate mechanism of repetitive syllable production in babbling might result from underlying oscillations of the neural motor system (12), which may also be one of the mechanisms underlying reduplication in bat pup babbling. Additionally, the repetition of syllables by bat pups might reflect the fact that several adult vocalization types ( fig. S4) contain repetitions of the same syllable types (7). Furthermore, the syllabic composition of pup babbling was mostly characterized by rhythmicity. Four of the five different syllable train categories ( fig. S5) found in babbling bouts had a regular beat ( Fig. 2F and table S4). Rhythmicity is also a salient characteristic of babbling in human infants (3).
Babbling bouts did not require a social context for production, even though pups often babbled during interactions with their mothers (see supplementary materials). Moreover, adultlike syllable types generated in babbling bouts did not elicit the same reactions that they would evoke when produced by adult bats (Fig. 2G). The absence of adult responses may be explained by the fact that the sender was a pup or by the different sequence of syllable types. Furthermore, the social context did not correspond to adult vocalization types. Syllables in human infant babbling also lack semantic information but can transmit affect to a caregiver (3). Furthermore, human infant babbling could serve as a fitness signal for caregivers (13)(14)(15) because babbling is a sign of typical child development. It is unclear whether babbling in S. bilineata pups may also signal fitness to mothers.
Irrespective of sex or regional origin, all pups babbled during ontogeny and produced undifferentiated protosyllables. We found no differences in age at babbling onset, duration of the babbling phase, and size of the pups' final syllable-type repertoire ( Fig. 2H and table S5). However, future investigations of more than two populations will be necessary to corroborate the universal occurrence of babbling in S. bilineata. Notably, both sexes acquired the syllable types constituting the adult male territorial song and produced them in the correct sequential order, even though only males sing as adults (5). Females' own experience of producing song syllables might facilitate their assessment of male song, thus influencing future mating decisions.
Our study provides the first formal analysis of bat pup babbling and reveals substantial parallels in multiple dimensions to babbling in human infants. The similarities in babbling features between two species with common traits such as laryngeal sound production, similar brain architecture, and vocal production learning offer future possibilities for understanding shared cognitive skills and neuromolecular foundations.