Introduction (from The Language of Animals)

You’d be hard pressed to find a person alive who didn’t grow up with talking animals. From 1930s Mickey Mouse cartoons to 1993’s “The Lion King,” from Puss in Boots to Brian Jacques’ mouse hero Mattimeo, children’s fiction in every medium abounds with animals talking to their own species, to other species and to humans. And the concept predates both cartoons and books; folktales from almost every culture contain talking animals.

Children soon learn that animals don’t talk. Or at least that humans can’t understand them. Or can they? Consider humankind’s best friend. First planting a cold, wet nose firmly against its master, it trots to the door, whining. Message heard and understood: “I want to go out.” A cat leaps on the desk at noon and walks back and forth between the computer keyboard and the monitor, then leads its owner to the empty cat food dish (possibly licked clean by the dog). Again, the animal has communicated to the human. (Humans clearly belong to the animal kingdom, but to avoid repetition, I’ll often use “animals” to mean “nonhuman animals.”)

Title page of the first edition of The Descent of Man, and Selection in Relation to Sex

Source: Wikipedia

In their own realm, animals also get their messages across. A male dragonfly swoops down on a female, grasping her for an aerial mating. Body size, shape and color patterns communicate her identity. With a dab of the right color paint, however, a researcher can fool the male. (More on dragonfly mating) Communicating by way of body shape or color obviously requires no awareness on the part of the sender, no intention to tell a story. Several other types of communication likewise require no consciousness on the part of the sender. Many female animals, from moths to naked mole rats and marmosets, use odor communication so powerful it can draw a male moth from miles away or prevent all but one of the female naked mole rats in a colony from ovulating.

These animals may have no conscious awareness of their body shape or odor. But in many other cases animals communicate more selectively, only in certain situations, for example. A common message content appears to be “Hi, I’m a male. Let’s mate.” Females, attracted by the signal, quietly approach the male. Given only that message, however, females would have little basis on which to choose mates. But in most species, the males also appear to add a superlative: “I’m not just a male, I’m a great male.” Do the females then pick the best advertiser? Charles Darwin addressed just this issue in his The Descent of Man and Selection in Relation to Sex, published in 1871. “There remains a question which has an all-important bearing on sexual selection, namely, does every male of the same species excite and attract the female equally? Or does she exert a choice, and prefer certain males?” Darwin’s contemporary and colleague Alfred Russel Wallace, who also published on natural selection, insisted that females could not choose mates because no female animal had the mental capacity to distinguish between males. Most scientists studying evolution of behavior today would disagree with Wallace. But the question of how female selection works remains controversial and complicated.

Evolutionary scientists propose several ways a female might make her choice of males, and several evolutionary rationales. In some species, the male provides food, help or protection, giving the female an immediate benefit; she therefore chooses the mate she thinks will best provide for her. If she’s right, her mate helps keep her healthy, and she produces healthy offspring who will carry her genes and her mate’s genes, including, presumably, good-provider genes. As a result, her genes stand a better chance in generations to come. But in other species, the male merely contributes sperm. And here the story gets more complicated.

A female may choose traits that correlate with good genes. She could do this in a number of ways, choosing the oldest male, for example—the one with the largest body, deepest voice, or most finely honed display. Older males have survived longer than younger males, and therefore may pass on survival genes. Or she may choose active or healthy looking males—the ones who dance most frenetically or sport the most pristine plumage. Healthy males would presumably contribute genes for healthiness. She could choose dominant males, those able to protect the largest, choicest or most highly decorated territory, or those most able to fight off other males.

In all these cases, researchers guess, the female trusts the signal. That could be a mistake. Imagine that peahens choose peacocks with longer tails. These males have obviously enjoyed good health in the months it takes to grow a resplendent tail, so they might contribute good genes for a variety of other traits. Female selection for longer tails fosters the evolution of longer and longer tails. At some point, the graph of increasing tail length crosses the graph of increasing male fitness. Beyond that point, tails become a drag on the male’s fitness, and no longer honestly advertise genetic quality. Where long tails once correlated with many good traits, they’ve become nothing more than empty advertising. The process has become a runaway feedback system. Most females continue to choose the longest-tailed males, even though a male with a slightly shorter tail represents a better genetic choice. Eventually, of course, the evolutionary system regains equilibrium, as females that include other characteristics in making their choice reproduce with slightly better success.

Some scientists speculate that for a signal to convey trustworthiness, it must obviously cost the male something. Called the “handicap principle,” this idea suggests that extravagant plumage, huge antlers or fantastic displays actually lower the viability of the male. Only males who can afford such luxury can pull off the display, the theory goes. Males with cheap displays may carry cheap genes, so females look for an expensive mating call, dance or plumage, one that appears of no immediate use to the male. Such costly communications may also signal health to predators. Certain springbucks, small antelopes of the Kalahari desert, communicate their excellent health to hunting dogs or hyenas with a curious behavior called stotting. Instead of running away flat out when they see one of these predators, some springbucks punctuate their escape with soaring leaps in the air. Jumping higher than their neighbors’ backs, with legs held stiff and parallel like a gymnast’s, the springbucks appear to say “There’s no use chasing me, I could obviously outrun you.” Overall, the handicap principle ensures the honesty of messages, some scientists contend, although any particular individual can still cheat.

The possibility that animals can deceive transcends mating calls, spilling over into communications with potential predators, sexual rivals and members of social groups.

Killdeer nest on rocky shores, exposed to predators. The gray and white bird nestles down, neatly camouflaged among the tan grass and gray pebbles. If you happen upon one, you might see a surprising spectacle. Instead of freezing or flushing, the Killdeer trots away at a moderate pace, with one wing held out and down at an awkward, broken-looking angle. Should you pick up the pace and follow—as a hungry raccoon might—you’ll find she keeps just out of reach, leading you ever farther from her nest. Turn back toward the nest and she’ll circle around and hobble all the more piteously. Finally, when she’s led you far enough astray, she rises like Phoenix, suddenly made whole.

Apparent deception does not require even the brain complexity of a bird. Fireflies present a fascinating drama of deception worthy of a mystery novel, complete with plot twists and killers. These small beetles, found world wide, emit light by mixing chemicals in a special organ in their abdomens. The male of each species blinks out a particular pattern of pulses, watches for the appropriate response from a female of the same species and then homes in on her beacon to mate.

The unwary male lighting next to a sexy-looking flashing light may get a deadly surprise, however. Predatory females of some species mimic the female flashes of other species, luring males to their deaths. These females only succeed about ten percent of the time, however, because males typically land a short distance from a beckoning female to more carefully assess her flashing code, or perhaps to double check her identity by sensing odors.

This hesitation aids certain firefly males, who appear to add another twist to the plot. They first approach a female of their own species and assure themselves of her identity. Then they begin imitating the flashes of predatory females. This causes competing males to hesitate longer, giving the first male time to lay a lasting claim to the female target.

All these animals may be doing what comes naturally, with no consciousness or intent, but they are not just playing a fixed behavioral tape. The Killdeer matches the pace of the supposed predator, and appears to monitor its reactions, overplaying her part if she’s not getting the attention she wants. And male fireflies send their own species-specific signal when attempting to communicate to a female and another species’ signal when attempting to scare off competing males. These behaviors imply at least a complex unconscious repertoire of communication. While it may be hard to imagine a firefly is conscious of cheating, and may be stretching a point to consider the killdeer fully aware of faking an injury, some instances of deception among great apes might change the mind of even the most ardent skeptic.

Frans B. M. de Waal [who wrote the foreword to The Language of Animals]studied a large colony of chimpanzees in the outdoor enclosure of the Burgers’ Zoo in Arnem, the Netherlands. In his book Chimpanzee Politics, he describes several observations of chimpanzees who appeared capable of calculated deception.

Two examples: Hurt in a fight with Nikkie, a chimpanzee named Yeroen began limping badly. But with careful observation, de Waal and his colleagues finally realized the ape only limped when he was within sight of Nikkie. As soon as he rounded a corner or circled behind the aggressor, the limp mysteriously disappeared.

Another chimp, named Puist, had developed the habit of faking a reconciliation gesture. After a fight, one chimpanzee will extend its hand, almost as if offering to shake. When Puist was getting nowhere in a fight, she would sometimes stop, approach slowly and extend her hand. When the opponent reciprocated, Puist would grab the hand and launch another attack. Watching chimpanzees and many other animals communicate, an observer cannot help but notice striking similarities between their behavior and ours. Vervet monkeys, for example, give one call when they see a snake and another when they see an eagle. Several animals communicate disingenuously. Bees, as simple as they are, appear to communicate information about distant nectar sites. Are these behaviors languages? No one equates bee dances or even chimpanzee hoots with human language. Our means of communication, no matter what culture we grow up in, far surpasses in complexity and subtlety that of any animal. But is the difference one of degree or kind?

Historically, philosophers have contended that language sets humankind apart from the simple beasts. Although all modern scientists fully accept Darwin’s assertion that most traits blend from simple to complex, they fall into two camps when it comes to language. One group insists human language bears little resemblance to animal communication, and resists the use of the word “language” to describe animal communication. These scholars—including many linguists—define “language” using features of human languages such as creativity, rules and meaning. Another group counters that animal communication grades from simple to very complex—human languages—just like any other trait. They point to monkey and chimpanzee behavior in the wild and to experiments in which great apes have learned to some extent to communicate with humans as evidence that the differences between human and animal languages are differences of degree and smaller than some would like to believe. No matter how exalted human language, it’s clear that we can communicate with some animals to some extent. Great apes have learned “languages” based on hand gestures and symbols. Parrots can learn to speak words, and even use those words to demonstrate feats of learning. Certainly a sharp “No!” carries some meaning to a dog. And many animals can learn respond to hand gestures and voice commands—we call this training. But another kind of experiment shows humans’ ability to convey meaning to animals of almost any kind. By recording animal sounds and playing them back, we can attract their attention or elicit the same behavior as the original call. In some cases researchers have modified signals and elicited modified behavior. These so-called “playback experiments” represent one of the most powerful tools scientists employ to begin understanding how animals really communicate.

Caveats and Confessions

The field of animal communication spans an incredibly wide range, from the color patterns of cuttlefish to the complex social life of dolphins. Every species that reproduces sexually must communicate at least enough so that it can mate. And the kinds of communication employed include all five senses we humans pay attention to, as well as some we are unable to detect, such as the electric sense of fish and the infrasound sense of whales. I have dipped into this sea of fascinating information and netted a few samples. I’ve necessarily left more out than I could include, hoping only to whet the reader’s appetite to learn more—by reading, to be sure, but even more importantly, by observing animals first hand. Finally, I confess I’ve made selections and written The Language of Animals as an admitted enthusiast. I’ve groomed a pet South American spider monkey, whistled to pet guinea pigs, monitored pet electric fish on my stereo, said “Do you want to go for a walk?” to numerous dogs and still discuss the state of the food bowl with cats. I sometimes spend sunny summer afternoons snapping pictures of spiders. I grew up loving animals, both fictional and real, and can fall into the gee-whiz mode with the best of them. But I also trained in neurobiology, a bench science much easier to control than language research and field observation. I hope both my love of animals and my bench-bred skepticism show through, as well as my firm belief that we can make the world a better place by learning about and conserving the creatures with whom we share this beautiful planet.