Homing in on bats' hearing

Head tilts, ear waggles, improve bats' hunting prowess

Mel Wohlgemuth always thought it was cute the way his pet pug, Willie, tilts his head from side to side. He never imagined the habit would inspire a scientific breakthrough.

Two years ago, Wohlgemuth, a behavioral neuroscientist at the Johns Hopkins University, was studying another species altogether — the common big brown bat — when he noticed the winged critters tilting their heads like Willie does. He decided to find out why.

A study he and a research team have just published found that the bats — and probably his dog — aren't cocking their heads just to be charming. They're enhancing their ability to hear and interpret sounds from the world around them, in large part to target prey.

The findings, which appear in the September issue of the open-source journal PLOS Biology, suggest that many animal species — dogs, bats and humans included — rely on more than pure ear power to carry out this key survival skill.

A well-calibrated turn of the head is a bigger help than you might think.

"It's an adorable behavior, and I was curious about the purpose," said Wohlgemuth, a postdoctoral fellow in the Krieger School of Arts and Sciences' department of psychological and brain sciences. "I wanted to know when bats were doing this and why. It turns out to be something they do when they're targeting prey. And our findings have applications across many species."

Scientists have long known that many of the world's 1,300 species of bats are among the most proficient creatures on earth at echolocation — a form of biological sonar in which an animal sends calls into the environment, then monitors the returning echoes as a way of nonvisual "seeing."

What sets Wohlgemuth's study apart is that he and his co-author, Johns Hopkins neuroscientist Cynthia Moss, are the first to investigate what role the pug-like head movements play in this complex process, particularly when it comes to hunting prey.

They also scrutinized a second bat habit — the way the animals wiggle their ears at the same time.

Their central finding: The bats vary the quality and rate of the "chirps" they send out based on how far they are from their prey, and the waggles and wiggles enhance their ability to read the echoes in ways scientists can measure.

"They change head and ear position to acquire more information, and it makes them better hunters," Wohlgemuth said.

Bats aren't the only animals to engage in "active sensing" — the practice of using motor skills to enhance the way they sample biologically relevant cues in their environment.

Pugs are likely using it when they tilt their heads, a movement that creates a sweep of the ears, enlarging their hearing arc.

Human beings do something similar, if on the visual plane, when they look at a subject from several points of view, developing a fuller perspective. They also do it when directing one ear toward a sound they want to hear, another way of expanding aural sweep.

Moss said echolocating bats are "the perfect models" for studying this phenomenon. They send out the very signals they are to collect, making it easier for researchers to isolate, track and quantify the variables.

It doesn't make studying them easy.

Bats are a crucial species around the world for the way they control the insect population — they're especially drawn to mosquitoes — and they're plentiful in Maryland, where the big brown bat (Eptesicus fuscus) is one of the more populous of 10 native breeds.

Armed with the requisite state permits, the researchers go out and capture bats that have nested in homes — something bats do in large numbers in certain areas of Baltimore County, including Dundalk and Essex, where there's plenty of standing water, and in the northern reaches with its preponderance of older homes.

Back at the Johns Hopkins Homewood campus, the team spent months designing the right experimental methods.

Wohlgemuth, Moss and their crew set up two windowless "flight rooms" in a basement suite known as Bat Labs.

In each room, they placed dozens of high-sensitivity microphones in strategic places to capture sound — the bats emit chirps at a higher frequency than humans can hear, and as many as 150 times per second — as well as four high-speed video cameras.

Placing reflective markers on the tips of the bats' ears allowed them to record the animals' speedy movements, chart them at precise intervals and determine how they synced with the sounds.

Finally, rather than letting the bats chase their prey (mealworms) as they would in nature, the team used Pavlovian conditioning to train each to remain standing on a platform.

They then drew the prey toward the stationary animal along fishing lines, recording how each bat reacted as the food arrived from differing angles, at differing speeds and in differing combinations.

What they learned surprised even Wohlgemuth.

When the bats "waggled" their heads, rocking them side to side, it turned out they were rotating their ears in a way that broadened their aural sampling range.

They also wiggled their ears independently. These movements — so subtle they can't be seen with the naked eye — added still more to the equation.

Slowing down the video to one-tenth its recorded speed, the team realized the bats were widening and narrowing the distance between the tips of their ears, again changing the size of their acoustic field of view.

When the prey was farthest away, the ears were at their most upright, their tips closest together. When the prey was nearer, the ears flattened, the tips growing wider apart.

Thousands of measurements showed they were carrying out two functions.

With more upright ears, they were "detecting" — trying to determine whether a potential meal was present at all. With the ears flattened, they were "localizing" — tracking the prey's smallest movements.

Both are essential to hunting — the first to identify the prey, the second to zero in for the kill — and the team found the bats could control the relationship between the two with mathematical precision as the distance to the prey varied.

The results "demonstrate that purposeful control over sonar sound production and reception can serve to improve acoustic cues for localization tasks," the authors wrote.

The finding emphasizes something that rarely has been shown so clearly; that bodily movement can be essential to sensory processing, whatever the species.

Wohlgemuth only wishes he knew whether it helps Willie. He didn't think to study the matter until after the pug, now 13, had lost nearly all his hearing.

Either way, the dog still tilts his head, and the owner still loves it.

"It's just an incredibly cute thing," Wohlgemuth said. "It's part of who he is."

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