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Variable food begging calls are harbingers of vocal learning.

Liu WC, Wada K, Nottebohm F - PLoS ONE (2009)

Bottom Line: The imitation of a memorized sound is a clear example of vocal learning, but is that when vocal learning starts?Here we use an ontogenetic approach to examine how vocal learning emerges in a songbird, the chipping sparrow.Electrolytic lesions of RA significantly reduce the variability of male calls.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Animal Behavior, The Rockefeller University, New York, New York, United States of America. liuw@mail.rockefeller.edu

ABSTRACT
Vocal learning has evolved in only a few groups of mammals and birds. The developmental and evolutionary origins of vocal learning remain unclear. The imitation of a memorized sound is a clear example of vocal learning, but is that when vocal learning starts? Here we use an ontogenetic approach to examine how vocal learning emerges in a songbird, the chipping sparrow. The first vocalizations of songbirds, food begging calls, were thought to be innate, and vocal learning emerges later during subsong, a behavior reminiscent of infant babbling. Here we report that the food begging calls of male sparrows show several characteristics associated with learned song: male begging calls are highly variable between individuals and are altered by deafening; the production of food begging calls induces c-fos expression in a forebrain motor nucleus, RA, that is involved with the production of learned song. Electrolytic lesions of RA significantly reduce the variability of male calls. The male begging calls are subsequently incorporated into subsong, which in turn transitions into recognizable attempts at vocal imitation. Females do not sing and their begging calls are not affected by deafening or RA lesion. Our results suggest that, in chipping sparrows, intact hearing can influence the quality of male begging calls, auditory-sensitive vocal variability during food begging calls is the first step in a modification of vocal output that eventually culminates with vocal imitation.

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Close resemblance between food begging calls and early subsong.(A) Food begging bouts (green bars) produced by a juvenile male at PHD25 and similar sounds in that bird's early subsong (red bars) at PHD 39.(B) A closer view of late begging calls and early subsong from the same male. (C). Three acoustic features (mean duration, Wiener entropy, mean frequency) of early subsong (n = 13 males at PHD 40) are more similar to those of late begging calls of males (n = 13; MANOVA, Wilk's Lamda = 0.086, P>0.05; Tukey post-hoc test)) than to those of females (n = 12) (80–85 call and subsong notes per bird) at PHD 25 (see Fig. S3 for detailed analysis).
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pone-0005929-g002: Close resemblance between food begging calls and early subsong.(A) Food begging bouts (green bars) produced by a juvenile male at PHD25 and similar sounds in that bird's early subsong (red bars) at PHD 39.(B) A closer view of late begging calls and early subsong from the same male. (C). Three acoustic features (mean duration, Wiener entropy, mean frequency) of early subsong (n = 13 males at PHD 40) are more similar to those of late begging calls of males (n = 13; MANOVA, Wilk's Lamda = 0.086, P>0.05; Tukey post-hoc test)) than to those of females (n = 12) (80–85 call and subsong notes per bird) at PHD 25 (see Fig. S3 for detailed analysis).

Mentions: The food begging calls of juvenile males closely resembled some of the sounds from early subsong, though the behavioral context was very different. Food begging stopped around PHD 30–36, and subsong was first recorded around PHD 28–40. Some males (2 of 13) started to produce subsong before they stopped food begging. Early subsong occurred when young males were well fed and, with their feathers fluffed and eyes closed, seemed to nap during the daytime (Movie S3). Unlike food begging, this subsong behavior was not directed at another individual. Subsong was much softer (mean amplitude = 31.6±3.5 dB) than begging calls (n = 5 males; 62.1±5.7 dB; n = 300 notes each) and showed greater variability in note structure (Fig. 2A). Some of the sounds of early subsong were very reminiscent of late begging calls in males (Audios S3, S4). This close similarity was quantified in two ways. First, five independent judges were asked to inspect visually sound-spectrogram of early subsong bouts and food begging calls of juvenile males (n = 5) and agreed that approximately 10–33% of early subsong was very similar to the late begging calls of males at PHD25, but not to those of female calls or to the begging calls of younger males (Fig. S3). Second, we used similarity scores from Sound Analysis Pro [25] to compare each male's begging calls and early subsong. Approximately 7–38% of the total duration of the sounds of subsong (range of all males) resembled that same male's begging calls at PHD25 with a similarity score of 67–85. None of the early subsong bouts matched male calls at PHD15 or female calls at PHD25 (Fig. S3). The “begging call-like” subsong matched late begging calls in almost all sound features (MANOVA, Wilk's Lamda = 0.086, P>0.05; Tukey post-hoc test) except the lower amplitude in subsong (Kolmogorov-Smirnov test, z = 4.18, P<0.001). The incidence of “begging call-like” sounds in subsong gradually subsided in the next few weeks. Females do not sing as adults and have no subsong.


Variable food begging calls are harbingers of vocal learning.

Liu WC, Wada K, Nottebohm F - PLoS ONE (2009)

Close resemblance between food begging calls and early subsong.(A) Food begging bouts (green bars) produced by a juvenile male at PHD25 and similar sounds in that bird's early subsong (red bars) at PHD 39.(B) A closer view of late begging calls and early subsong from the same male. (C). Three acoustic features (mean duration, Wiener entropy, mean frequency) of early subsong (n = 13 males at PHD 40) are more similar to those of late begging calls of males (n = 13; MANOVA, Wilk's Lamda = 0.086, P>0.05; Tukey post-hoc test)) than to those of females (n = 12) (80–85 call and subsong notes per bird) at PHD 25 (see Fig. S3 for detailed analysis).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2691483&req=5

pone-0005929-g002: Close resemblance between food begging calls and early subsong.(A) Food begging bouts (green bars) produced by a juvenile male at PHD25 and similar sounds in that bird's early subsong (red bars) at PHD 39.(B) A closer view of late begging calls and early subsong from the same male. (C). Three acoustic features (mean duration, Wiener entropy, mean frequency) of early subsong (n = 13 males at PHD 40) are more similar to those of late begging calls of males (n = 13; MANOVA, Wilk's Lamda = 0.086, P>0.05; Tukey post-hoc test)) than to those of females (n = 12) (80–85 call and subsong notes per bird) at PHD 25 (see Fig. S3 for detailed analysis).
Mentions: The food begging calls of juvenile males closely resembled some of the sounds from early subsong, though the behavioral context was very different. Food begging stopped around PHD 30–36, and subsong was first recorded around PHD 28–40. Some males (2 of 13) started to produce subsong before they stopped food begging. Early subsong occurred when young males were well fed and, with their feathers fluffed and eyes closed, seemed to nap during the daytime (Movie S3). Unlike food begging, this subsong behavior was not directed at another individual. Subsong was much softer (mean amplitude = 31.6±3.5 dB) than begging calls (n = 5 males; 62.1±5.7 dB; n = 300 notes each) and showed greater variability in note structure (Fig. 2A). Some of the sounds of early subsong were very reminiscent of late begging calls in males (Audios S3, S4). This close similarity was quantified in two ways. First, five independent judges were asked to inspect visually sound-spectrogram of early subsong bouts and food begging calls of juvenile males (n = 5) and agreed that approximately 10–33% of early subsong was very similar to the late begging calls of males at PHD25, but not to those of female calls or to the begging calls of younger males (Fig. S3). Second, we used similarity scores from Sound Analysis Pro [25] to compare each male's begging calls and early subsong. Approximately 7–38% of the total duration of the sounds of subsong (range of all males) resembled that same male's begging calls at PHD25 with a similarity score of 67–85. None of the early subsong bouts matched male calls at PHD15 or female calls at PHD25 (Fig. S3). The “begging call-like” subsong matched late begging calls in almost all sound features (MANOVA, Wilk's Lamda = 0.086, P>0.05; Tukey post-hoc test) except the lower amplitude in subsong (Kolmogorov-Smirnov test, z = 4.18, P<0.001). The incidence of “begging call-like” sounds in subsong gradually subsided in the next few weeks. Females do not sing as adults and have no subsong.

Bottom Line: The imitation of a memorized sound is a clear example of vocal learning, but is that when vocal learning starts?Here we use an ontogenetic approach to examine how vocal learning emerges in a songbird, the chipping sparrow.Electrolytic lesions of RA significantly reduce the variability of male calls.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Animal Behavior, The Rockefeller University, New York, New York, United States of America. liuw@mail.rockefeller.edu

ABSTRACT
Vocal learning has evolved in only a few groups of mammals and birds. The developmental and evolutionary origins of vocal learning remain unclear. The imitation of a memorized sound is a clear example of vocal learning, but is that when vocal learning starts? Here we use an ontogenetic approach to examine how vocal learning emerges in a songbird, the chipping sparrow. The first vocalizations of songbirds, food begging calls, were thought to be innate, and vocal learning emerges later during subsong, a behavior reminiscent of infant babbling. Here we report that the food begging calls of male sparrows show several characteristics associated with learned song: male begging calls are highly variable between individuals and are altered by deafening; the production of food begging calls induces c-fos expression in a forebrain motor nucleus, RA, that is involved with the production of learned song. Electrolytic lesions of RA significantly reduce the variability of male calls. The male begging calls are subsequently incorporated into subsong, which in turn transitions into recognizable attempts at vocal imitation. Females do not sing and their begging calls are not affected by deafening or RA lesion. Our results suggest that, in chipping sparrows, intact hearing can influence the quality of male begging calls, auditory-sensitive vocal variability during food begging calls is the first step in a modification of vocal output that eventually culminates with vocal imitation.

Show MeSH
Related in: MedlinePlus