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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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Sexual dimorphism of food begging calls.(A) The food begging calls of the females are more stereotyped than those of males at PHD20. Each call note (light-blue bar) is repeated 3–7 times in a rendition (orange bar). Prior to begging calls, juveniles produce “chip” contact calls (red bars) as a parent approaches. (B) The begging calls of each female shown came from a different clutch (females 2–5), but males 2–5 are siblings from the same clutch at PHD 20. (C) Higher call variability in juvenile males (n = 13) than females (n = 12) at PHD 20 is seen as the scatter plot distribution of entries for six acoustic features: duration, pitch, Wiener entropy, frequency modulation (FM), pitch goodness, and mean frequency. Male calls were significantly different from female calls in these features (see Fig. S2). Each dot represents a female (blue) or male (red) call note.
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pone-0005929-g001: Sexual dimorphism of food begging calls.(A) The food begging calls of the females are more stereotyped than those of males at PHD20. Each call note (light-blue bar) is repeated 3–7 times in a rendition (orange bar). Prior to begging calls, juveniles produce “chip” contact calls (red bars) as a parent approaches. (B) The begging calls of each female shown came from a different clutch (females 2–5), but males 2–5 are siblings from the same clutch at PHD 20. (C) Higher call variability in juvenile males (n = 13) than females (n = 12) at PHD 20 is seen as the scatter plot distribution of entries for six acoustic features: duration, pitch, Wiener entropy, frequency modulation (FM), pitch goodness, and mean frequency. Male calls were significantly different from female calls in these features (see Fig. S2). Each dot represents a female (blue) or male (red) call note.

Mentions: The begging calls of chipping sparrows became audible at post-hatching day (PHD) 3–5. Most juveniles reached independence and stopped begging at PHD 30–36. We define food begging calls as the vocalizations produced by a juvenile when food is presented a few inches in front of it (Movies S1, S2). Initially, the food begging calls were high-pitched pure tones (Fig. S1). After fledging (PHD 9–11), two different call types emerged: the food begging calls of fledglings and the “chip” contact call (Fig. 1A). Each individual bird produced a single type of food begging call, though the calling intensity (i.e., the number of repeated notes per food-begging bout), the calling rate (number of call renditions per unit of time), and amplitude varied with the degree of hunger. “Chip” Contact calls were emitted prior to the food begging calls as parents approached. This contact call is functionally and morphologically similar to the contact call of adults.


Variable food begging calls are harbingers of vocal learning.

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

Sexual dimorphism of food begging calls.(A) The food begging calls of the females are more stereotyped than those of males at PHD20. Each call note (light-blue bar) is repeated 3–7 times in a rendition (orange bar). Prior to begging calls, juveniles produce “chip” contact calls (red bars) as a parent approaches. (B) The begging calls of each female shown came from a different clutch (females 2–5), but males 2–5 are siblings from the same clutch at PHD 20. (C) Higher call variability in juvenile males (n = 13) than females (n = 12) at PHD 20 is seen as the scatter plot distribution of entries for six acoustic features: duration, pitch, Wiener entropy, frequency modulation (FM), pitch goodness, and mean frequency. Male calls were significantly different from female calls in these features (see Fig. S2). Each dot represents a female (blue) or male (red) call note.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2691483&req=5

pone-0005929-g001: Sexual dimorphism of food begging calls.(A) The food begging calls of the females are more stereotyped than those of males at PHD20. Each call note (light-blue bar) is repeated 3–7 times in a rendition (orange bar). Prior to begging calls, juveniles produce “chip” contact calls (red bars) as a parent approaches. (B) The begging calls of each female shown came from a different clutch (females 2–5), but males 2–5 are siblings from the same clutch at PHD 20. (C) Higher call variability in juvenile males (n = 13) than females (n = 12) at PHD 20 is seen as the scatter plot distribution of entries for six acoustic features: duration, pitch, Wiener entropy, frequency modulation (FM), pitch goodness, and mean frequency. Male calls were significantly different from female calls in these features (see Fig. S2). Each dot represents a female (blue) or male (red) call note.
Mentions: The begging calls of chipping sparrows became audible at post-hatching day (PHD) 3–5. Most juveniles reached independence and stopped begging at PHD 30–36. We define food begging calls as the vocalizations produced by a juvenile when food is presented a few inches in front of it (Movies S1, S2). Initially, the food begging calls were high-pitched pure tones (Fig. S1). After fledging (PHD 9–11), two different call types emerged: the food begging calls of fledglings and the “chip” contact call (Fig. 1A). Each individual bird produced a single type of food begging call, though the calling intensity (i.e., the number of repeated notes per food-begging bout), the calling rate (number of call renditions per unit of time), and amplitude varied with the degree of hunger. “Chip” Contact calls were emitted prior to the food begging calls as parents approached. This contact call is functionally and morphologically similar to the contact call of adults.

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