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Wingéd chorale
In birdsong, CAS biologist hears more than male voices

By Tim Stoddard

AMouth agape, this young cardinal knows how to say, “Feed me.” But it will take several months for it to learn how to sing like an adult. In her lab, Ayako Yamaguchi has found that female cardinals learn to sing about three times faster than males, but that males ultimately acquire a wider repertoire of songs. Photo by Ayako Yamaguchi

Boston’s flowerbeds are still days away from a burst of daffodils, but the feathered harbingers of spring arrived on campus weeks ago, belting out their melodies from tree branches and powerlines. Songbirds like the Northern cardinal have been adding their voices to BU’s urban symphony, and for Ayako Yamaguchi, a cardinal’s song is more than a pleasant assurance of spring: it’s a biological puzzle that may shed light on how birds and whales and humans learn to vocalize.

Yamaguchi, who recently joined the CAS biology department as an assistant professor, has been listening closely to young cardinals, and she’s found that the drab brown females learn to sing three times faster than the flashy red males. It’s the most dramatic example of learning disparities between male and female animals found to date, she says, and it’s leading to new insights into the sexual differences in singing.

“ People have studied birdsong for about 50 years now,” Yamaguchi says, “and so we know a lot about how and when birds learn to sing, and how accurately they can imitate songs. But we don’t know anything about how females learn songs because all the research is done on males.”

Male birds have taken center stage, she says, because in temperate zones, there are only a few species in which both sexes sing. And since the majority of biologists live and work in temperate zones, it’s natural that the literature has focused on male singers. But that leaves a significant hole in the literature concerning female songbirds, which is especially acute in the tropics, where singing is common in both males and females.

As a graduate student, Yamaguchi decided to blaze a new trail in birdsong research by comparing male and female vocal learning in the Northern cardinal, one of the few temperate species in which both males and females sing. She collected chicks in the Arizona desert and carried them in a cotton-ball-padded yogurt container back to her laboratory at the University of California, Davis, where she began the laborious process of raising the little birds. “You have to feed them every half hour from six in the morning to eight at night for the first two weeks of their lives,” she says. “It’s a pretty intensive effort.”

The chicks grew up in special sound chambers with microphones and speakers that play back the songs of adult cardinals. It takes about a year for a cardinal to learn to sing properly, Yamaguchi says, and like human infants acquiring speech, young songbirds learn to sing by imitating adults. The early months are part of the so-called sensitive phase, when the chicks don’t say anything, but listen attentively to singing adults to memorize their songs. Then the practicing begins. “Their initial attempts are pretty miserable,” she says, “but they practice and practice until it matches the memory that was formed earlier during the sensitive phase.”

Yamaguchi found that male and female cardinals actually have sexually distinctive voices, like sopranos and baritones. Even an avid birdwatcher would be strapped to pick out a male cardinal’s song from a female’s, however, but in 1998 Yamaguchi analyzed the songs of juvenile birds and found that the females sing with more overtones, creating a slightly nasal sound. Young males also go through a nasal, warbly phase as their testosterone kicks in, she says, but it’s as though the females continue to sing with an adolescent male’s voice.

More important, Yamaguchi discovered that female cardinals memorize adult songs three times faster than males. While both sexes ultimately learned the same number of song types, the females’ sensitive phase was only a third as long as the males’. The different learning rates may reflect an evolutionary adaptation. Like other songbirds, juvenile cardinals disperse from their parents’ territory about 45 days after hatching to establish their own turf before their first breeding season. Away from their natal nest, the young cardinals are suddenly immersed in the new song dialects of other adult cardinals. It appears that females lose the ability to learn new dialects when they disperse, while males are able to learn them and “fit in” with their new neighbors.

“ It might be that males retain the ability to learn songs longer than females so that they can have a better chance of establishing territory in a new area,” Yamaguchi says. “For males, song-matching and fitting into the crowd in a new place are really important, while they’re not for females.” It’s not clear why female cardinals have a shorter window of vocal learning, she says, but then again, “we don’t really know why females sing at all, or how they use their songs.” One hypothesis, she says, is that females sing as a species identification tool, a greeting card to male cardinals that says, “I’m an eligible mate; come court me.” Other researchers have proposed that female cardinals sing to shoo away brightly colored mates from the nest when a predator is nearby, warning the males not to attract attention to the vulnerable chicks. “I know that female cardinals also use songs in aggressive behavior,” Yamaguchi says. “I’ve seen females battling each other in the field, and they’re singing the whole time as they bang into each other.”

Pavarotti of the pond

	A frog in the hand: In Ayako Yamaguchi’s lab, croaking African clawed frogs are shedding light on the complex crooning of songbirds like the Northern cardinal. Next spring she will raise cardinal chicks in her lab to investigate the different ways males and females learn to sing. Photo by Kalman Zabarsky

Yamaguchi is still feathering her lab at BU, but already she’s found a home for the African clawed frogs that she has recently begun studying along with songbirds. She wants to better understand the neurological changes in male and female cardinals as they acquire song, but it’s difficult to track changes in a bird’s brain through time. Instead, she has turned to a simpler singer, the African clawed frog. Both male and female frogs vocalize underwater with a single pair of muscles in the larynx. Male frogs purr like a revving engine, while females pipe out a slower-paced “crick . . . crick . . . crick.” In her postdoctoral work at Columbia University, Yamaguchi discovered that both male and female frogs were sending the same neural signals from their brains to their voice boxes to make the sounds. But the male frog brains somehow send the “crick” message faster and more accurately, so that their laryngeal muscles contract at a faster rate than those of females.

“ That finding was quite new, and it was quite a tour de force to demonstrate it so clearly in frogs,” says Peter Marler, a songbird expert at U.C. Davis and Yamaguchi’s Ph.D. advisor. “Ayako’s great achievement was to show that it’s not sufficient simply to look at the vocal apparatus to explain the difference between male and female calling. You have to look back up into the brain for a full understanding.”

At the larger scale, Yamaguchi’s work may someday have applications for other species that learn to vocalize, such as Homo sapiens. Human infants learn to speak the same way that cardinal chicks do, and the cardinal results also parallel the subtle but consistent gender differences in human speech acquisition. “Ultimately, the question is, how do male and female brains work differently?” she says.

It’s a fitting question, considering that Yamaguchi became interested in language acquisition as she herself was learning to speak English at the age of 15. Born and raised in Tokyo, she spent a year of high school on an exchange program in southern Utah. “At the beginning, I couldn’t understand a word they were saying,” she says without a trace of accent. “Then slowly I began to understand and imitate the vocalizations that people were making, and I thought it was such a fascinating process, converting auditory information into motor output.”

Returning to Tokyo, Yamaguchi enrolled in the prestigious Japan Women’s University, where studying biology was something of a challenge. “The university prides itself on producing good wives and wise mothers,” she says with an ironic grin. “Eighty percent of the prime ministers’ wives are from our college.” A skilled experimentalist, Yamaguchi admits that cooking and cleaning are not her forte.

Yamaguchi’s lab is unusually quiet these days, but she expects that to change next spring when she resumes her cardinal work. The new cardinals will learn to sing in a sound isolation room in the basement of the biological sciences building, hopefully out of earshot of faculty and students upstairs. “When they start singing, the sound pressure is about 90 decibels at one meter away,” she says, “which is like standing on a subway platform and having a train pass by.”

4 April 2003
Boston University
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