Around 1934, when Tinbergen was working in the Department of Zoology at Leiden University in Holland, he and a student, Joost ter Pelkwijk, started to wonder about the red color on the three-spined stickleback.
“In springtime, male sticklebacks develop ‘nuptial colors’ of a bright-red belly and throat and defend their territories,” says Anderson. “The male builds a nest inside its territory and will court and guide females, which have a silvery color, toward it. If she enters and lays her eggs, he will follow her and fertilize them. Then he will protect the eggs from marauders (often other sticklebacks) and guard the young.” The sticklebacks would attack any other males that venture into their territory. “Niko had set up aquarium tanks containing sticklebacks alongside the windows in his laboratory at Leiden University,” Anderson says. “In one of them was a single male in nuptial colours. Pelk and Niko both noticed that this male would regularly start a frantic head-down display, holding itself in the peculiar vertical position designed to tell intruders to get out of his territory, even though there was no other male nearby. The attack was aimed toward the window, and it wasn’t long before they figured out that it began whenever the bright-red post van drove past the window on the way to deliver the letters.”
This led Pelkwijk and Tinbergen to do a famous set of experiments showing that you could provoke a stickleback to attack simply by showing it a red object. “These initial experiments by Tinbergen and others led to a whole body of theory on ‘sign stimuli’ and ‘innate releasing mechanisms,’” says Anderson. More recent work suggests that red alone won’t annoy every male, but once one gets annoyed, others may join in the agitation. Perhaps it’s not all that surprising that red agitates a male stickleback. Certainly, red is a color that elicits a kind of annoyance that matadors in Spanish bull rings are professionally familiar with.
Skunk spray that reminds us of rotting food, red mail trucks that remind fish of fighting, fingernails on a chalkboard that remind us of a scream—these annoyances may have something in common. The unpleasantness is linked to aversive responses that have evolved to keep us alive. The annoyances remind us of something we’re programmed to avoid, triggering a strong reaction. They are a case of mistaken identity—we can’t distinguish between the threat and the thing that mimics the threat.
Rachel Herz doesn’t buy the evolutionary theory about skunks. In fact, she thinks we’re born without any smell preferences at all. Herz nicely details her argument in The Scent of Desire, but the crux of it is that all of a person’s smell likes and dislikes are learned—including an aversion to skunk spray. “I know it’s a startling statement to make,” she says.
Take the smell of rotten eggs—it’s hard to imagine not having a gag reflex to that smell, but Herz says that babies show no aversion to the odor. Young children show no preference for the smell of bananas over the smell of poop. Nursing babies have been shown to actually prefer garlic-scented milk. As for skunks, Herz herself likes the smell. She says that her skunk spray predilection comes from an experience she had as a child: she was out on a sunny summer day with her mother, who exclaimed, “Isn’t that smell nice?” when the skunk spray smell wafted through the air. Herz has liked the odor ever since. Eric Block, who specializes in sulfur compounds, has a similarly warm feeling about skunk spray: “I don’t mind it that much because when I smell it, it kind of reminds me of the work that I do.”
In small doses, some thiols are widely pleasing, even to nonchemists. “You can have pleasant-tasting thiols,” says Block. For example, a freshly opened container of coffee smells wonderful, thanks to a particular thiol. “Thiols at very low concentrations, including methanethiol, are actually very important in the taste of wine and the odor of different types of wine. At high concentrations, the perception is skunky or stinky or garbagey or something like that.” For smells, too, it seems that intensity matters.
Detection also matters, says Herz. Not all humans are thought to have the same odor receptors, meaning that not everyone will smell the same scents. This variation in receptors can make people sensitive to certain scents. For example, if the smell of skunks is particularly annoying to you, it may be because you have more receptors that are sensitive to thiols. What might smell moderately strong to one person could make you gag if you have more receptors for that odor. “It has to do with the intensity,” Herz says. “Even your favorite piece of music is aversive if it’s blaring.” Herz says that this is an instance where there are innate differences in response to smell.
Herz argues that judgments about particular smells come less from an inherent like or dislike but more from the context. She has investigated how association affects our perception of a scent. In one particularly memorable study published in the journal Perception, Herz and Julia von Clef asked eighty undergraduates to do a smell test on some “ambiguous” scents and rate their pleasantness.{21} The scents were labeled differently in various sessions. For example, violet leaf was labeled “fresh cucumber” in one session and “mildew” in another; pine oil was “Christmas tree” in one and “spray disinfectant” in another. The real kicker was a 1:1 chemical composition of isovaleric and butyric acids that was labeled “parmesan cheese” in one experiment and “vomit” in another.
The researchers found that the labels made a big difference between annoying and appetizing. People strongly liked the smell of what they thought was parmesan but were repelled by the same odor when they were told it was vomit. This fits in with Herz’s theory that our preference for smells is largely dependent on learning and context. On the matter of skunk spray, Herz argues that certain animals, those specifically adapted to a particular habitat, do seem to be born with innate olfactory responses. She argues that humans, as generalists, are different. We’re better off being able to learn quickly whether a smell is bad or good, rather than being preprogrammed to avoid a smell.
Herz suggests that our collective dislike of skunk spray may also be related to the fact that it’s irritating physically. Smells can have feelings associated with them. Menthol feels cool. Ammonia burns. Skunk spray hurts. The feelings associated with smells are picked up by nerve cells in our noses and eyes—these receptors are responsible for the tears we cry over raw onions. Herz suggests that for compounds such as ammonia and thiols in skunk spray, we don’t separate the smell from the sensation. “In actuality, what we’re being repelled by or annoyed by is the irritancy, but we say we don’t like the ‘odor.’”
Skunk spray becomes more threatening in very high doses. There have been reports of dogs dying as a result of being sprayed, according to Wood and Dragoo, although this appears to have more to do with the consistency of the spray than its scent—the oil is thought to coat their lungs. Humans have suffered, too. In 1881, Dr. W. B. Conway, at the Virginia Agricultural and Mechanical College in Blacksburg, recounted a story in the Virginia Medical Monthly about the unfortunate victim of a practical joke. A few college boys “secured a two-ounce bottle of the perfume from the skunk,” Conway wrote. The boys entered the victim’s room, held him down, and forced him to sniff the spray straight from the bottle. “I could not ascertain what amount was administered,” Conway wrote. “However, when I reached him I found the following symptoms: A total unconsciousness, relaxation of the muscular system, extremities cool, pupils natural, breathing normal, pulse 65, temperature 94; in which condition he remained for one hour.” To treat the comalike symptoms, the doctor “administered small quantities of whisky at short intervals per orem, with some difficulty getting him to swallow.” It took about an hour and who knows how many whiskeys, but the boy was eventually revived. The take-home point: like many annoyances, skunk spray is usually irritating but can become sickening in high doses.