Nothing pleasant about the smell of fear

Published 5:00 am Wednesday, August 15, 2012

Deseada Parejo, a biologist at the Arid Zones Experimental Research Station in Almeria, Spain, was studying family dynamics behavior in Eurasian rollers — spectacular jay-size birds with long, slender tails and the Cray-Pas colors of parakeets. On removing one of the nestlings for a standard check of size and weight, she practically jumped at its horror-film response: The tiny chick gaped its mouth wide and vomited up a big dose of sticky orange liquid, enough to fill half a teaspoon.

Parejo touched a second chick, a third, a sixth, and got the same expulsory retort.

“I have worked with many other bird species,” she said, “but I never found anything similar to this vomiting behavior before.”

Not only that: The fluid had a distinctive, evolving odor.

“It’s like orange juice at first,” she said. “Then it begins to smell like insects, like the prey the parents provide.”

In the current issue of Biology Letters, Parejo and her colleagues describe their study of this noteworthy aroma, which they designate the roller nestlings’ “smell of fear.” The researchers said that while the reflux reflex might well serve as a defense mechanism — helping to repel nest predators like snakes and rodents — they were interested in a different question: whether the parents could detect the olfactory cry of alarm, and if so, how they reacted.

The answer to the first question was yes. But the parental response to the eau of offspring terror was anything but heroic; instead, it was a bit like those childhood nightmares, where the louder you cry out to Mom and Dad in a crowd, the faster they leave you behind.

Fear factors

The new findings add to the growing evidence that many animals can smell one another’s fear, including species not known for their bloodhound powers.

Birds and humans in particular were long thought to rely on vision and hearing rather than smell when sizing up the world and its ambient threats. Yet recent research reveals that birds have a nose for news after all, that people are deeply affected by odors in ways they often are not consciously aware of, and that one class of odor likely to impinge on both humans and birds is the scent of a fellow’s despair. In human studies, the sweat of frightened people has been shown to cause anxiety and heightened vigilance, and even to enhance cognitive performance on tests.

Biologists have long known of fear factors in nature — chemical signals released by a distressed individual, either deliberately or inadvertently, that end up inciting similar displays of fear or agitation in recipients. Ants disturbed in their nest produce alarm pheromones that rally colony defenses. If air is blown over the cage of a rat as it receives an electric shock to the foot, rodents downwind of the jolting event react with a full-blown stress response, as if they, too, had been shocked.

Karl von Frisch, the legendary Austrian honeybee researcher, discovered in the 1930s that the skin of an injured minnow oozed into the water a substance he called Schreckstoff (“fright stuff”), which prompted other minnows in the vicinity to immediately flee the site of obvious antiminnow intentions. This year, researchers finally isolated from the mucus of fish skin the active ingredient of Schreckstoff: chains of sugars called chondroitins that are so potent at repelling fish they just might make a great gag addition to your loved one’s next fishing trip.

Injured plants also release alarm signals through air and soil that can be construed as evidence of vegetal despair, or at least a reminder that no life form likes being eaten, even by vegans.

Avian olfaction

Birds, by contrast, were thought to express their fear by freezing, swooping or screeching, and they were considered to have little if any sense of smell, a misconception thought to date back to poorly designed experiments by the naturalist and artist John James Audubon in the 19th century. Besides, said Julie Hagelin, a senior research scientist with the Institute of Arctic Biology at the University of Alaska, Fairbanks, “birds don’t show behaviors that would lead you to think they’re scent-marking” like a dog.

Yet recent neuroanatomy studies have revealed that birds have olfactory equipment that rivals any mammal’s, and in some cases surpasses it. Kiwis, for example, have nostrils at the tip of the beak and one of the largest olfactory bulbs known, relative to brain size.

Behavioral research has likewise yielded proof of avian olfaction.

“The crested auks that I study smell like tangerine during the breeding season,” Hagelin said, “and they spend a lot of time sniffing each other around the nape of the neck.”

The aroma of cat scat wafting up from the base of a feeder is all it takes to keep certain songbirds away, while among domestic chicks, one bird will react excitedly to the smell of feces from a fearful peer, but only if both the smelled and smeller are eating a natural diet of insects and greenery.

“If you feed them Purina chicken chow, you wipe out this effect,” said Hagelin, who cautioned that the chick results have yet to be published.

A natural and varied diet also contributes to the roller nestling’s smell of fear. Parejo points out that roller parents will feed their chicks certain toxic prey items that other birds avoid, like centipedes and spiders, and she speculates that one reason the nestlings vomit when frightened is to tell would-be predators, “I am chemically well-armed.”

Whether the strategy works against a peckish snake remains to be demonstrated, but the parents clearly eavesdrop on the conversation. In the newly reported experiments, the researchers applied either orange vomit or lemon essence to the inner rim of the nest boxes; they found that parents took significantly longer to re-enter the nest, and fed their young less often, when the vomit odor was present.

Human responses

People, too, can smell trouble’s track marks. Reporting in the journal Neuroendocrinology Letters, Karl Grammer of the University of Vienna and his colleagues found that subjects who sniffed underarm pads from women who had just watched either a neutral documentary about train travel or the horror film “Candyman” rated the latter’s odor as “significantly stronger and more unpleasant” and claimed it reminded them of “aggression.”

In other studies, olfaction operates behind the scenes. As they described in the journal Chemical Senses, Denise Chen of Baylor College of Medicine and her co-workers gathered sweat samples from male and female undergraduates who watched either a documentary or a scary film — including that old roller bird classic “The Exorcist.” The swabs were then placed under the noses of students, who expressed only vague opinions about odors (“smells like the ocean”). Yet when they took a series of cognitive tests in which they had to determine whether pairs of words flashed on the screen were related or unrelated, the sweat of fear seemed to improve their performance.

The results are preliminary, and researchers have no idea what the human equivalent of Schreckstoff might be, or whether it has potential as an aid for the SATs. Just keep it away from your parents, kids, or you may not eat for a week.

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