Research

Projects

Signaling strategies

In many species of animals, males spend large amounts of energy and become more exposed to predators while signalling to attract females to mate. That is the case of frog calling. In many species, advertisement calling is by far the most energetically expensive activity that males engage in. Tropical species can have very prolonged breeding seasons, and males have been show to be limited in calling by their energetic reserves. 

A male frog can distribute his effort over a number of dimensions of calling (sound intensity, call duration, call rate, hours per night, etc), but he cannot maximize all such dimensions at the same time.

We are interested in quantifying the calling strategy in the main dimensions that vary during calling in nature. This will allow us to better predict how frogs adjust their reproductive behaviors to changes made in the environment - an important insight for wildlife management.

Specializations of the vocal apparatus

Human speech is acoustically very elaborate, and demands a versatile vocal apparatus. Frogs, in contrast, tend to produce very simple, repetitive sounds. They usually produce 2-4 types of calls with a fixed structure, but the vast majority of the vocal activity involves males producing the species-specific advertisement call to attract females for mating.

While the calls are simple, there are more than 5,000 species of frogs, and extensive acoustic variability is found among species. This provides an opportunity to study structural specializations of the calling apparatus that maximize its ability to produce each type of sound.

We study the anatomy and performance of the frog calling apparatus across species, to bring novel insight into the design and evolution of vocal systems.

Calling with the mouth closed

While most frogs are known to produce incredibly loud calls, they do so having their mouths and nares shut - the air flows into the vocal sac. Why would they not open their mouths to call?

Several possible explanations have been offered, including:

* Amplification by the vocal sac

* More efficient use of energy

* Faster reinflation

* Reduced dehydration

* The inflating sac can serve as a visual signal

We artificially activated the larynx of euthanized animals and compared the sounds produced having the mouth open or closed We found that with the mouth open, the energy of the call would become spread over a wide range of frequencies. Closure of the mouth filters out the acoustic energy from low and high frequencies, and it increases the amplitude at intermediate ones. By calling with the mouth closed, frogs can concentrate their vocal output into a narrow frequency range, making their signals more effective in species recognition.

Call complexity and laryngeal anatomy

In another study, we examined the túngara frog, which is odd for producing mating calls with a facultatively added note that makes the call acoustically more complex. This species is also odd for having part of its larynx greatly expanded. It was tempting to assume that the laryngeal expansion was related to the call complexity, but a causal relation had not been shown.

We recorded frogs calling in nature, surgically removed the laryngeal expansions, and after recovery, we recorded the new calls produced by the frogs. The operated frogs were able to produce normal calls, and add facultative notes, but the acoustic complexity was lacking from the facultative notes. This revealed a rare case in which a specialization of the laryngeal morphology can be tied to the production of a specific sound. Such finding has implications in the current understanding of the evolution of acoustic complexity, and the mechanics of vocalization.

Sensitivity to ultrasound

Until recently, frogs were thought not to be able to hear sounds with frequencies above 5-8 kHz (humans hear up to 22 kHz). This picture changed when Feng and collaborators (2006) found that the Chinese concave-eared torrent frog can hear ultrasound up to 34 kHz. This was an amazing 5-7 fold expansion of the known hearing range for frogs.

While many mammals (bats, dolphins, rodents) can hear high frequencies, their eardrums are connected to the inner ear by three hard ossicles. In contrast, no other tetrapod was known to hear above 10-12 kHz, and non-mammal eardrums are connected to the inner-ear by a bone and a cartilage. It was believed that the cartilage, being soft, would absorb high frequencies. So how could the Chinese frog hear ultrasound?

To answer this question we went to China and played calibrated tones to the frog in the lab, while using a Doppler laser vibrometer to measure the motion of the eardrum. (This is a weak laser that does not harm the frog). The experiment showed that the eardrums of the frog actually respond very well to ultrasound, in contrast with other well known frogs.

We are also measuring the vibration of the cartilage and the bone inside the ear of these and other frogs in response to sound, and characterizing the anatomy of their ears. Such measurements are revealing several anatomical specializations in the ultrasound-hearing frogs, that allow their ears to opperate effectively at high frequencies. This research aims at answering a question about design and another one about ecology/evolution. DESIGN: What sensor design features of the ear are varied among animals in nature to adjust the range of operation of the ears?

ECOLOGY/EVOLUTION: What are the environmental pressures that most commonly lead to adaptation of the hearing range?

Control of the Eustachian tube

The mouths of tetrapods connect to the air-filled space behind the eardrums through a passage called Eustachian tube. In mammals, this passage remains collapsed until we yawn or swallow. In frogs, the Eustachian tubes were believed to remain permanently open, until we recently discovered that some frogs can close them.

We also found that closure of the Eustachian tubes shifted the hearing sensitivity of the frogs to high frequencies. Eustachian tube closure, turned out to be a novel mechanism of behavioral adjustment of the frequency range of hearing. It parallels the acoustic reflex, in which contraction of muscles in the middle ear restrict the motion of the eardrum when exposed to loud sound. But Eustachian tube closure has a different mechanism: it changes the resistance of the air behind the eardrum to bulging of the membrane.