Vocal plasticity in harbour seal pups

Abstract

Vocal plasticity can occur in response to environmental and biological factors, including conspecifics' vocalizations and noise. Pinnipeds are one of the few mammalian groups capable of vocal learning, and are therefore relevant to understanding the evolution of vocal plasticity in humans and other animals. Here, we investigate the vocal plasticity of harbour seals ( Phoca vitulina ), a species with vocal learning abilities observed in adulthood but not puppyhood. To evaluate early mammalian vocal development, we tested 1–3 weeks-old seal pups. We tailored noise playbacks to this species and age to induce seal pups to shift their fundamental frequency ( f 0 ), rather than adapt call amplitude or temporal characteristics. We exposed individual pups to low- and high-intensity bandpass-filtered noise, which spanned—and masked—their typical range of f 0 ; simultaneously, we recorded pups' spontaneous calls. Unlike most mammals, pups modified their vocalizations by lowering their f 0 in response to increased noise. This modulation was precise and adapted to the particular experimental manipulation of the noise condition. In addition, higher levels of noise induced less dispersion around the mean f 0 , suggesting that pups may have actively focused their phonatory efforts to target lower frequencies. Noise did not seem to affect call amplitude. However, one seal showed two characteristics of the Lombard effect known for human speech in noise: significant increase in call amplitude and flattening of spectral tilt. Our relatively low noise levels may have favoured f 0 modulation while inhibiting amplitude adjustments. This lowering of f 0 is unusual, as most animals commonly display no such f 0 shift. Our data represent a relatively rare case in mammalian neonates, and have implications for the evolution of vocal plasticity and vocal learning across species, including humans. This article is part of the theme issue ‘Voice modulation: from origin and mechanism to social impact (Part I)’.

Vocal tract allometry in a mammalian vocal learner

“…As shown here, by testing for allometric relationships between body size and vocal tract structures, one can start to disentangle the respective contributions of vocal anatomy and vocal motor control in shaping acoustic signals. We find that harbour seals are mechanistically constrained by their vocal anatomy, and their large vocal flexibility (Ralls et al, 1985;Borda et al, 2021), which may result in the production of dishonest signals, thus points towards extensive volitional control over their vocalisations. In brief, we provide support for the morphology vs. learning hypothesis, showing however that this relation may be mediated by ontogeny.…”

“…In one special case, a human-raised harbour seal, named Hoover, was found capable of mimicking human speech sounds (Ralls et al, 1985). In a more recent study on harbour seal pups, young animals were found capable of lowering their fundamental frequency (f 0 ) in the presence of background noise (Torres Borda et al, 2021). Do the environmental noise conditions in which vocalisations are produced have a stronger influence on the f 0 values than body size?…”

“…Do the environmental noise conditions in which vocalisations are produced have a stronger influence on the f 0 values than body size? To address this, we complemented acoustic data from Torres Borda and colleagues (2021) with body mass information and reanalysed it to show that acoustic allometric relationships do indeed break down in this species due to the large vocal plasticity observed within individuals (see Figure 2, its caption and detailed explanations in the Supplement). These re-analyses indicate that, also within-species, individual harbour seals may sound bigger or smaller than predicted by body size.…”

“…Based on previous literature, we expect to find allometry between body size and vocal tract structures that are surrounded—and hence constrained—by bony structures, such as vocal tract length. However, based on harbour seals’ vocal learning abilities (Ralls et al, 1985; Torres Borda et al, 2021; Janik and Slater, 1997), we expect their vocal flexibility to offer favourable grounds to find deviations from body size allometry for vocal tract components surrounded by cartilage, such as the trachea and vocal fold length.…”

Voice modulation: from origin and mechanism to social impact

“…The remaining seven contributions in Part 1 are empirical. Torres Borda et al [4] (critical topics (ii) and (iii)) present evidence of the early emergence of vocal plasticity in an aquatic mammal, the infant harbour seal. Their results show that these pinniped pups, known to be capable of vocal learning in adulthood, can already modulate calls in response to noise at one to three weeks of age.…”