Vocal control by the common marmoset in the presence of interfering noise

Abstract

The natural environment is inherently noisy with acoustic interferences. It is, therefore, beneficial for a species to modify its vocal production to effectively communicate in the presence of interfering noises. Non-human primates have been traditionally considered to possess limited voluntary vocal control, but little is known about their ability to modify vocal behavior when encountering interfering noises. Here we tested the ability of the common marmoset (Callithrix jacchus) to control the initiation of vocalizations and maintain vocal interactions between pairs in an acoustic environment in which the length and predictability (periodic or random aperiodic occurrences) of interfering noise bursts were varied. Despite the presence of interfering noise, the marmosets continued to engage in antiphonal calling behavior. Results showed that the overwhelming majority of calls were initiated during silence gaps even when the length of the silence gap following each noise burst was unpredictable. During the periodic noise conditions, as the length of the silence gap decreased, the latency between the end of noise burst and call onset decreased significantly. In contrast, when presented with aperiodic noise bursts, the marmosets chose to call predominantly during long (4 and 8 s) over short (2 s) silence gaps. In the 8 s periodic noise conditions, a marmoset pair either initiated both calls of an antiphonal exchange within the same silence gap or exchanged calls in two consecutive silence gaps. Our findings provide compelling evidence that common marmosets are capable of modifying their vocal production according to the dynamics of their acoustic environment during vocal communication.

Fig. 1.

Acoustic recordings of marmoset phee calls made during different noise conditions: (A) periodic: 4 s, (B) aperiodic: predictable, (C) aperiodic: unpredictable. The latency between noise offset and call onset is indicated in B. (D) Left: amplitude of a three-phrase phee call recorded during a baseline session (top), overlapped with noise (middle) and de-noised (bottom). The average power of the phee call was 30 dB SPL. Right: spectrograms of the waveforms shown to the left. After de-noising, the soft phee call is clearly detectable.

Fig. 2.

Percentage of calls initiated per session under the different noise conditions. The majority of calls in the aperiodic conditions were initiated in 4 and 8 s silent gaps. Data shown are means ± s.e.m. (N=8 subjects). Statistically significant differences with Bonferroni correction are indicated by an asterisk (*P<0.05). (A) Percentage of calls per session during the different periodic noise conditions. (B) Percentage of calls in a given predictable session initiated in 2, 4 or 8 s silent gaps. t-test results: 2 s vs 4 s (t₇=3.45, P<0.017), 4 s vs 8 s (t₇=6.87, P<0.001), 2 s vs 8 s (t₇=9.68, P<0.001). (C) Percentage of calls in a given unpredictable session initiated in 2, 4 or 8 s silent gaps. t-test results: 2 s vs 4 s (t₇=2.87, P=0.024), 4 s vs 8 s (t₇=2.57, P=0.037), 2 s vs 8 s (t₇=4.50, P<0.017).

Fig. 3.

Latency between noise offset and call onset for the different noise conditions. Data shown are means ± s.e.m. (N=8 subjects). Statistically significant differences with Bonferroni correction are indicated by an asterisk (*P<0.05). (A) Comparison of the latency for the different noise conditions. Data shown are for the periodic 2 s, 4 s and 8 s, aperiodic predictable (pred.) and aperiodic unpredictable (unpred.) conditions. The latency between all pairs of condition was significantly different except for predictable vs unpredictable and periodic 4 s vs unpredictable. (B) Comparison of the coefficient of variation of the latency for the different noise conditions. (C) Comparison of the latency following a 2, 4 and 8 s noise pulse in the aperiodic predictable conditions. These data were regrouped from aperiodic sequences, i.e. all calls initiated in 2 s silent intervals were grouped together, etc. Repeated-measures ANOVA showed a significant difference in mean following a 2, 4 and 8 s noise pulse (F_2,14=14.806, P<0.001; Mauchly's W=0.715, P=0.365). Paired t-test results: 2 s vs 4 s (t₇=7.35, P<0.001), 2 s vs 8 s (t₇=13.76, P<0.001), 4 s vs 8 s (t₇=6.44, P<0.001). Shapiro–Wilk normality test results: 2 s (W=0.959, P=0.804), 4 s (W=0.977, P=0.946), 8 s (W=0.923, P=0.456). Levene's test (F=3.2493, P=0.06) indicates equal variance. (D) Latency for calls made in the aperiodic: unpredictable session plotted against the preceding noise pulse length. Repeated-measures ANOVA showed significant differences between call latencies (F_2,14=13.623, P<0.001; Mauchly's W=0.417, P=0.072). The mean latency did not significantly vary for 2 and 4 s noise pulses (latency=4 s) but was significantly lower following an 8 s noise pulse (latency=2.3 s). Paired t-test results: 2 s vs 4 s (t₇=0.0112, P=0.914), 2 s vs 8 s (t₇=6.25, P<0.001), 4 s vs 8 s (t₇=5.31, P<0.001). Shapiro–Wilk normality test results: 2 s (W=0.823, P=0.051), 4 s (W=0.904, P=0.31), 8 s (W=0.921, P=0.44). Levene's test (F=1.6503, P=0.2159) indicates equal variance.

Fig. 4.

Antiphonal calling in the presence of periodic noise. (A) Example of antiphonal call exchange between caller 1 and caller 2 within the same silent gaps in the periodic 8 s condition. (B) Example of antiphonal call exchange between consecutive silent gaps in the periodic 8 s condition. (C) Comparison of the periodic 8 s and baseline antiphonal call delays of all pairs in 2 s bins. Means ± s.e.m. of percent calls are shown with statistically significant differences between periodic 8 s noise condition and baseline (*P<0.05) indicated by an asterisk.

Fig. 5.

Antiphonal and individual calling parameters. Statistically significant differences between the noise and baseline are marked by an asterisk (*P<0.05). (A) Antiphonal call latencies for the different noise conditions and baseline. t-test results of the comparison of each noise condition with the baseline are: 2 s vs baseline (t₇=3.16, P=0.016), 4 s vs baseline (t₇=6.045, P=0.001), 8 s vs baseline (t₇=7.23, P<0.001), predictable vs baseline (t₇=4.453, P=0.003), and unpredictable vs baseline (t₇=4.272, P=0.004). (B) Comparison of the calling rate of marmosets in the different noise conditions with the baseline. t-test results: 2 s vs baseline (t₇=6.06, P=0.001), 4 s vs baseline (t₇=3.756, P=0.007), 8 s vs baseline (t₇=5.06, P=0.001), predictable vs baseline (t₇=2.826, P=0.026), unpredictable vs baseline (t₇=1.935, P=0.094). (C) Percentage of overlapped short-latency and long-latency call exchanges in noise conditions and at baseline. (D) Percentage of overlapped calls in the different noise conditions.