The Little Frogs With the Big Sounds

Amolops tormotus is a frog species found only in two regions of China. Tau Hua Creek in central China, habitat to Amolops tormotus, was a noisy and wild locale for Beckman researcher Al Feng to conduct his experiments.
Amolops tormotus is a frog species found only in two regions of China. Tau Hua Creek in central China, habitat to Amolops tormotus, was a noisy and wild locale for Beckman researcher Al Feng to conduct his experiments.

Al Feng’s ultrasonic frog: Beckman researcher leads team that makes groundbreaking discovery.

The scientists’ surroundings were picturesque in daylight but especially hazardous at night: mountain runoff water rushing between steep, forested banks that hindered moonlight from reaching the many rocks and boulders dotting the creek bed. But it wasn’t the beauty of the central China resort area or a possible misstep leading to injury that occupied Albert Feng’s mind. It was a mounting sense of frustration.

Feng and his fellow researchers had used helmet lights and flashlights to navigate the rocks in Tau Hua Creek’s cool, noisy waters for almost a week, recording instruments in hand, listening in vain for the mating calls of a unique species of frog known as Amolops tormotus. They had located the small, tan amphibians whose Chinese name means sunken ear frog among rocks in the creek, and waited patiently night after night in that summer of 2000, hoping for a chorus of what scientists refer to as advertisement calls from the males.

Finally, one night the scientists heard sharp, musical sounds they took to be coming from birds – an assumption, it turned out, the locals had also made when they heard those same calls. As the sounds of the creek’s other creatures began to die down in the latenight hours, the bird-like calls stood out to the bored researchers. Their curiosity aroused, they temporarily abandoned the quarry that brought them halfway around the world and headed to the creek bank where the sounds were coming from.

“The first thing we noticed is these aren’t birds because they are calling from the ground,” Feng said. “They turned out to be frogs. Next thing we know, those are our frogs.”

The team got its recordings, but with them came a surprise. The readouts of the frog calls showed unlimited variations and the frequencies on the high end appeared to extend into the ultrasound range – a discovery that contradicted the biology textbooks. Amphibians weren’t thought to produce ultrasound (frequencies greater than 20kHz), except perhaps as a fluke byproduct of other communication. The results produced a paper, a story in Nature’s online “Science Update” and media attention from NPR to the BBC for the little frogs capable of producing limitless sound patterns and ultrasonic harmonies. What they didn’t show was how far in the ultrasonic range the calls were, or answer the larger question: were the ultrasonic calls just a byproduct of an ordinary mating call or were they used for communication, as is the case with only a few groups of animals in nature.

Fast forward to May of 2002. Feng and his team return to the area, focusing their efforts on detecting ultrasonic calls from the Amolops. This time they brought with them German biologist Hans-Ulrich Schnitzler, a preeminent expert in ultrasound recording of animals in their natural habitat who focuses on bats with ultrasonic echolocation capabilities. The return visit provided a repeat pattern of initial frustration followed by some truly unexpected findings, thanks to Schnitzler’s equipment and adventurous spirit. The results of their research, detailed in a 2004 journal article by the researchers, showed that both songbirds from the area and the Amolops produced ultrasound, with the frogs’ calls extending into the high ultrasonic range.

Then in May of 2005, lugging state-of-theart, PC-based recording equipment created by Schnitzler, Feng and his associates returned to the Huangshan Hot Springs to determine for good whether the little frog with no visible ears could prove the textbooks wrong. What they found should open up a new way of thinking about ultrasonic communication among vertebrates.

A few years before, Cornell biology professor Kraig Adler had directed Feng and his UCLA colleague Peter Narins to Amolops tormotus because it did not have external eardrums like all other frog species; rather, it possessed the unique anatomical feature of an ear canal with recessed eardrums. That fact alone made the Chinese frog worthy of further investigation for a researcher like Feng, whose focus at the Beckman Institute for Advanced Science and Technology is on the neural basis of sound pattern recognition in frogs and bats. Amolops tormotus, or concaveear torrent frog, are located in just two regions of China, both of which feature bodies of water. The rainy season in the frog’s habitats is known to turn meandering creeks into boisterous venues for wildlife – creating such a cacophony, in fact, that Feng and his colleagues often had to shout to one another in order to be heard.

In the spring of 2002, it wasn’t the silence of the Amolops that was frustrating the team, but one of Huangshan’s downpours that prevented a ny serious research work getting done. Feng, the team’s leader, decided to call it a night. But Uli, as the outdoorsy Schnitzler is known, reveled at the idea of some rainsoaked research and set off to record bats in a nearby cave with equipment that detects ultrasound up to 128 kHz. A few minutes later, an animated Schnitzler returned with some astounding news. The Amolops were in full refrain, and their calls were off the ultrasonic charts.

“About 15 minutes later he came back and said ‘come on up, you guys have to come up, these guys are calling like crazy.” Feng said. “And not only that, the call frequencies were extending furthest into the ultrasonic range. It went beyond the capacity of Uli’s equipment. He said ‘I cannot believe that this can happen.’”

The German biologist was shocked, as was Feng.

“Bats can do this, dolphins and whales, among underwater mammals, can do this. But in the vertebrates, it was typically known that they are limited to these small groups of animals that can perform this,” Feng said. “Frogs definitely would not be taken into consideration as a remote possibility. So this came as shocking news to us. We were stunned, in fact.”

The team had another new bit of research to report, but was still left with the question of whether this remarkable ultrasonic capability was a byproduct or actual communication. Schnitzler went back to his lab to custom build a PC-based recording device and an ultrasonic microphone to capture sounds that would then be digitalized using a converter and saved as wavefiles. The device Schnitzler created not only could record at the high ultrasonic range Amolops was capable of, but also could play back those recorded sounds for use as a stimulus.

Another expedition in the summer of 2005 followed and, using digital wavefiles of Amolops advertising calls, Feng’s team played the calls through loudspeakers. They got “immediate” feedback, Feng said.

The group was able to see, from real-time readouts, the stimulus calls were quickly followed by antiphonal, or prominent, responses, thus demonstrating a temporal relationship between the playback calls and the calls that followed. Some of the responses were in the audible range and some in the ultrasonic range, but the fact a chorus was formed based on an ultrasonic stimulus left no doubt about the purpose of the sounds. The frogs were in fact using ultrasound for communication – and at very high frequencies.

The discovery goes beyond one little frog in China. It has the potential to change not only the way scientists think about amphibians, but other species as well. Feng said this discovery means that ultrasound communication will be likely be found in other creatures once scientists are open to the possibility. “We’ll reevaluate everything.”

That reevaluation could include investigating the calls of a species of warbler songbirds found along the same streams as the Amolops.

“In the 2002 paper we found some birds in the same region of China produce some sounds in the ultrasonic range,” Feng said. “I would not be surprised if this bird also uses ultrasound to communicate. If frogs make this adaptation, it makes sense that other creatures in the area (also do). We have seen evidence like this, the parallel evolutions where different species converge into a similar solution.”

Feng said bats use ultrasonic communication in order to avoid cluttering the communication channels, but for frogs and birds to develop the same function is extraordinary.

“They shift the hearing to the upper frequencies in order to get around the sounds produced by other creatures,” Feng said. “This frog is unusual in that regard. The (frogs and birds) converged on the same solution. We have seen that before but this is probably a novel form of parallel evolution because this is totally unexpected.”

Feng said the Amolops’ development of ultrasonic capability probably came about as a result of having to communicate in the noisy environment of rushing waters. In their 2002 Naturwissenschaften article, the team reported that calling was more active when temperature and humidity were high, and found that “ambient noise from the stream at the calling sites was intense, especially after a heavy rainfall.”

“Clearly there are several ways to get around the noisy background,” Feng said. “One of them is to shift the frequency beyond the spectrum of the background noise. This is seemingly what this particular species is doing.”

The Amolops males were also found to have a “rich vocal repertoire” and each individual male had his own distinctive call.

Feng believes ultrasonic communication explains why Amolops developed ear canals and recessed eardrums. He said that in order for the frogs to receive very high frequencies they must have thin eardrums (larger eardrums couldn’t vibrate at those frequencies), but that thinness also makes the eardrum vulnerable. So an ear canal developed, leading to the recessed eardrum. At the same time, the recessed eardrum puts the eardrum much closer to the inner ear, reducing the mass of the middle ear bones that mediate transmission of sound energy from the eardrum to the inner ear for sound detection.

It was that recessed eardrum that caught Feng’s attention to begin with. Feng came to China to study a frog with an unusual morphology. He left it this past year with a new perspective on what animals are capable of. The various expeditions culminated with a report in the March 16th issue of Nature, “Ultrasonic Communication in Frogs”, by Feng, Narins, et al.

But this most recent report is not the end for Feng, or other researchers willing to walk through the same door. Now that Amolops has been found to have this capacity, what other species can also communicate at the ultrasonic level? Feng expects the work of his team to spur other research.

“I’m sure it will because now we really have to change the complete modus operandi of (this research),” he said. “This is no longer the domain of limited groups of animals.”

But in order to find out which animals, it takes the right equipment.

“This is the thing: unless you have a device to look for this, and if you don’t look for this, you’ll never find it,” Feng said.

And it takes the right amount of patience. Feng still remembers those nights back in 2000 waiting in the rocks of Tau Hua Creek for the calls that never came. “That was very frustrating because we came all this way to find them, wanting to study them and they didn’t show any overt behavior.”

But the team’s dedication paid off – that and a willingness to look and listen where no one had before. Feng said the locals were surprised to learn the unique sounds they heard at night were coming from frogs.

“They thought they were little birds,” he said. “All of us thought the same thing too. They’re hard to find if you don’t look for them.”

But they did look for them, often by ignoring the advice of workers at the Huangshan Hot Springs hotel who warned of the creek’s possible dangers. It could be raining on the hilltops, they said, and someone in the creek might not know it until floodwater wa s crashing down on them. Watermarks on the boulders 10 feet high and more above the creek bed testified to what happens when Tau Hua Creek floods.

But the danger or frustration isn’t what Feng remembers most about his quest to understand why one little frog in China has distinctive ears.

“This was a fun trip, particularly when exploring an unknown, that’s always fun,” he said. “There’s always a reason why things are different and when you finally understand it, it’s just a rewarding experience.

“You explore an unknown and are finally able to explain it. That’s just tremendous satisfaction for me.”

This article is part of the Spring 2006 Synergy Issue, a publication of the Communications Office of the Beckman Institute.