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Females' Siren Song Initiates Courtship Duets In African Frogs, Columbia Biologists Find

February 17, 1998

The female of a species of South African frog doesn't wait for suitors to make the first move, according to new research by Columbia University biologists. As her eggs become ready to fertilize, she begins a clicking song that initiates a courtship duet with a nearby male that helps the partners find each other.

The female's aphrodisiac song, called "rapping," is a rapid series of loud clicks that sound like a Geiger counter exposed to a lode of uranium. It is among the rare instances in the animal kingdom where the female takes the first step.

Conventional wisdom in biology is that males advertise for mates and females answer: peacocks display, peahens admire; cocks crow, hens attend. It is extremely uncommon for females to initiate courtship, and "advertisement songs" that indicate receptivity had been thought to be the exclusive province of males. The male South African clawed frog, Xenopus laevis, had been thought to advertise his availability first, with a distinctive trill, and then to grab in succession the nearest females, releasing those that were not ready to lay eggs.

The new work, reported in the Feb. 17 issue of the Proceedings of the National Academy of Sciences, contradicts this view. The research, which also sheds light on how hormones may affect the nervous system, was conducted by Darcy B. Kelley, professor of biological sciences; Martha L. Tobias, senior research scientist, and Sandya S. Viswanathan, a graduate student in neurobiology and behavior, all at Columbia.

A female frog faces an urgent problem: there is a span of only about 24 hours in which her eggs are ready to receive sperm. She must attract a suitor during that period, or lose her progeny. Mating takes place at night in murky ponds crammed with frogs, making it difficult for receptive females to locate males, even though the males vocalize continuously during breeding season. If a receptive female can't locate the male, she sings her rapping song; the male responds with a different song, an answer trill, and mating follows. If a male approaches an unreceptive female, she responds with a different song, a slow, monotonous ticking, which silences him.

"Our best guess is that duetting makes it clear to both parts of the receptive pair who and where the other member is," said Dr. Tobias, who conducted the initial field work near Cape Town. "One could think of the female's advertisement call as a general love song and the male's answer call as a serenade to a specific love object."

Because visual cues are absent or nearly so and the mating period is short, vocalization is an ideal way for female frogs to find a mate. The authors suggest these factors may have necessitated a reciprocal signaling system in this species.

The team's first experiment, performed by Dr. Tobias in Cape Town, involved placing receptive male and female frogs in a concrete pond on opposite sides of a visually opaque but acoustically transparent barrier and using a hydrophone to record their calls. Receptive females swam directly towards vocalizing males, and on reaching the barrier began rapping. That song had a dramatic effect on males, which launched into intense bouts of answer trilling and swam rapidly in search of the source.

The research team was not certain that duetting was what brought male and female frogs together until they recorded the female rapping song and played it to male frogs in a fiberglass tank. The males again responded with an answer trill and tried to swim toward the sound, in one case even attempting to mate with the loudspeaker. Ms. Viswanathan conducted these experiments at Columbia's biological sciences department.

Dr. Tobias discovered the female's mating call and coined the term for it. "When Darcy came to South Africa, I demonstrated the female behavior and song to her. That night the four of us, husbands included, sat around thinking up names for the song," she said. "I hit on 'rapping' because it does mimic the sound, which is something like a Geiger counter."

Professor Kelley had already shown that the Xenopus male's brain and male muscles are specialized for his prolonged courtship songs and that the secretion of male sex hormones, androgens, are responsible for establishing the numbers and types of cells required for the vocalizations. Connections between male vocal neurons and muscle fibers is weak, but strengthen with use. Dr. Tobias had demonstrated that an isolated male vocal organ can be stimulated to produce the advertisement call. Though the researchers understood the neural and anatomical basis for frog songs, they had no idea how the animals used the songs until they were able to conduct field work.

The discovery of rapping highlights the role of another hormone, estrogen, produced by females. Estrogen circulating in sexually receptive females acts on the neurons that control their mating song to strengthen the connection between neurons and vocal muscles, the scientists have found. "The effect resembles the action of estrogen in the mammalian central nervous system," Professor Kelley said. "That's a topic of considerable interest to scientists examining hormone effects on brain function, since estrogen has already been shown to delay the onset of Alzheimer's disease and improve verbal memory in women."

The work was supported by the National Institutes of Health.

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Columbia University

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