Just before midnight, I crawl off my hammock and slip quietly from under the blessed drapes of mosquito netting. The kerosene lanterns have been dimmed to barely a flicker across the long raised wooden platform that serves as our base camp in the tropical rain forest of northwestern Peru. The platform is in the center of a clearing next to the bank of a small tributary that feeds into the Napo River half a mile away. I arrived with four other journalists and a guide late in the afternoon after hiking through the muddy and tangled jungle since early morning. We have joined two scientists, a few camp cooks, and the drunken pilot of a Cessna seaplane, who arrived just before dinner. The pilot is supposed to give us a flyover of the region first thing after breakfast. As much Johnny Walker Red scotch as he was putting away tonight, he'll still be drunk when we take off on the river early in the morning. The bush pilot's creed is, If you can't fly drunk, you can't fly.
This is my first trip to the Amazon rain forest. The closest I have come to a jungle until now is the tangled thicket of the Ozarks, where I grew up. Surprisingly, there are a lot of similarities, especially in the number of things that bite, sting, scratch, and burn. At the moment, the others in the expedition party are snoring. But that isn't why I'm awake. There's a raucous party going on -- with lots of wild action by the strange and wondrous creatures all around our campsite. The night is teeming with sounds that seem louder and more intriguing than anything I have ever heard.
A minute ago, high in the canopy just beyond the camp's perimeter, something big crashed through the leaves. The only creature large enough around here to make such noise is a sloth. True to its name, it does not seem to be in much of a hurry. Bats have been fluttering since dusk through the rafters of the thatched roof above the platform. Earlier this evening, one swooped down and snatched a tarantula that was crawling up a colleague's mosquito netting. We could hear a soft crunch as the bat caught the spider with its teeth and darted off with its dinner into the night.
Beyond the camp, in vibrant surround sound, tree frogs and insects are laying down a soulful, energetic chorus like a choir at an old-fashioned Southern tent revival. Unfamiliar birds and nocturnal monkeys overlay the chorus with melodies and their own unique lyrics. This is one party I am not going to miss despite the rather condescending warning of the scientists not to leave camp alone at night. We could get lost or worse, they cautioned. I spend quite a bit of time in the field, but no matter where I travel, scientists tend to treat journalists like bad children who need constant supervision. Their admonishment only heightens my resolve to sneak out of camp.
The main attraction of this remote spot in the jungle is a canopy walkway constructed with ladders and suspension bridges that leads 115 feet straight up to the tops of the trees. Ordinarily, getting to the upper canopy entails climbing with harnesses and ropes. This is no simple task and usually involves close encounters of the unpleasant kind with nasty things that sting, burn, and bite. The canopy walkway, which bears a strong resemblance to the Swiss family Robinson's tree house, is a vast improvement on grappling and slapping one's way up. As far as I know, only a few of these walkways exist in the world. Tonight, this one is going to be my stairway to heaven.
I am on a mission and have a woefully short time to fulfill it: to learn how animals communicate with each other and what they spend so much time chattering to each other about. At this point, my quest seems absolutely overwhelming. Real experts devote entire careers to studying a single species of animal and are still left with many more questions than answers at the end of the day. My head is full of questions, too, which I plan to explore and explain in this book: If animal behavior is mostly instinctual, as scientists generally thought for more than a hundred years, why do animals need to communicate? If animals are thinking creatures and capable of emotions, as a growing number of scientists now believe, do their signals convey information (similar to our words)? Or are animals merely snarling or cooing to manipulate each other's behavior to get something they want (as we also often do)? How did the colorful, noisy, and smelly signals of the animal kingdom arise in the first place? Is any animal system of communication similar to human language? Do animals ever lie or attempt to deceive each other when communicating? Do the chirps, barks, and roars of different species have anything in common or follow predictable rules or patterns? Can a bird understand a monkey? Do species learn to communicate or is it all programmed by genes? To what extent is human communication, both verbal and nonverbal, programmed into our genes?
Scientists have been asking questions like these and working hard at finding the answers for more than a century, but there have been an enormous number of recent discoveries about animal communication. Studies on communication among tree frogs alone could fill a book. The eminent sociobiologist E. O. Wilson and the entomologist Bert Hölldobler produced a 732-page tome devoted to ants. I have three books in my home library on cichlid fishes, seven devoted to primates, five on dogs, more than a dozen on various species of birds. Most books focus on a single behavior, such as courtship rituals among birds, or the social behavior of primates, or the chemical signals of insects.
Yet surprisingly few books written for the general public have focused on the great range of animal communication. Usually, these books devote only a chapter or two to songs, dances, and scents. So my challenge here is to draw from the wealth of research conducted by hundreds of scientists and present the bigger picture of animal talk in the wild. The Amazon rain forest seemed like the best place to get a full immersion in nature and to begin eavesdropping on some animal conversations.
The few remaining unspoiled rain forests of the world are nature's Manhattan, London, and Tokyo -- bustling organic metropolises with their own laws that govern every creature equally from conception through life and into death. The laws of nature demand procreation and a fight for survival, but the means developed to achieve those ends are tremendously varied. Mother Nature has fostered all manner of societies, cultures, learning, gaming, altruism, deception, cooperation, competition, industries, arms races, and intelligence. Look closely at any habitat and you can find daily dramas involving struggles between predators and prey, elaborate courtships, covert copulations, sibling rivalries, struggles for dominance, defense of territories, and many, many opportunities to arrive at a premature death. The same dramas are played out all over the world in every environment, from the deep ocean vents where microscopic life may have begun to the lawns and shrubs only a few steps away in the backyard.
Communication between all of the earth's creatures makes these dramas possible. Indeed, communication is the glue of animal societies. Without a means of communicating, no life, including the simplest single-celled organisms, could exist. Communication, like the tango, takes two. And it requires a signal, which can be anything from the release of chemicals between colonizing bacteria, to the come-hither flashes between male and female fireflies in the backyard, to the "let's go" rumble of African elephants, to the "signature" whistles of dolphins, to a dog barking simply to be let outside.
Over the course of our journey we will explore the origins of communication and how all of the marvelous signals employed by animals have developed. We will also look at why scientists think the way they do about animals. A pretty big divide separates scientists and laypeople, especially in their perspectives on animal behaviors. Yet, as ordinary people and pet owners become more informed and as scientists come to better appreciate the genuine intelligence of their animal subjects, both groups are moving toward a middle ground.
Before we head off into the jungle and climb the canopy walkway, we ought to know what scientists mean when they talk about animal communication. The basic textbook definition of animal communication taught to most undergraduate students states that it is "the provision of information by a sender to a receiver, and the subsequent use of that information by the receiver in deciding how to respond. The vehicle that provides the information is called the signal." One example of animal communication is the exchange between songbirds in a tree in the backyard. The male songbird is usually the sender. He sings his repertoire of songs, which is the signal, to a female songbird that has lighted on a nearby branch to listen. She is the receiver. The information would be something contained in the male's songs that helps the female decide whether the singer is a suitable mate. An exception to this male-dominated art and science is the northern cardinal -- each sex sings to the other, and they even seem to duet. My mom's fat little Chihuahua, Taco, is another example. Taco has a habit of running to my mom and barking in a particular manner whenever my dad does not hang up his jacket when he comes home from work. Taco is the sender. Mom is the receiver, and the information is that dad left his jacket on the bed. (How my mom knows Taco's bark carries this specific meaning, however, is a mystery.)
E. O. Wilson takes the definition a bit further in Sociobiology: The New Synthesis. Wilson defines communication this way: "Biological communication is the action on the part of one organism (or cell) that alters the probability pattern of behavior in another organism (or cell) in a fashion adaptive to either one or both of the participants. By adaptive I mean that the signaling, or the response, or both, have been genetically programmed to some extent by natural selection. Communication is neither the signal by itself nor the response; it is instead the relationship between the two."
The exchange of chemical signals between bacteria is the oldest form of communication on the planet and provides a good example of Wilson's definition. For pathogenic bacteria to become harmful to us humans, they first need to reach a critical mass, which they do by communicating with each other essentially to take a head count. A single E. coli bacterium -- the type that naturally lives in our gut but sometimes contaminates foods -- will release a chemical signal that sends the message "I am here." If pathogenic bacteria are present, the message will cause them to release a similar signal that says "I'm here, too." If the bacteria sense that their numbers are strong enough to ward off an attack by the host's immune system, they will all respond by releasing their toxins into the host's cells. The signals are genetically programmed and create a dynamic relationship between the senders and receivers, a type of bacterial communication known as quorum sensing.
All types of chemical signals, including those used by animals to attract mates, are adaptive, by Wilson's definition. Chemical signals originated with the first group of bacteria that appeared on the young earth, about 3.8 billion years ago. Thanks to their highly effective signaling, bacteria often function as a type of superorganism and are one of the most successful forms of life on earth. They are also the only life-form that appears capable of living elsewhere in our solar system.
The signaling that allowed colonies of bacteria to thrive in all types of environments, from ocean vents to glacier ice, eventually gave rise to the cell-to-cell communication that made possible the evolution of multicelled organisms. This "adaptive" communication has facilitated the incredible success of the earth's insects, including the 8,800 species of ants, which Wilson and Hölldobler say constitute an amazing 15 percent of the earth's biomass. In fact, Wilson developed his definition of communication from the study of ants, which have evolved a complex social system by using specific chemical signals with unambiguous meanings. Any given chemical signal produced by a sender will elicit a specific, invariable response from a receiver. For example, if an invader enters a colony of fire ants, sentries will release a chemical alarm that summons other members of the colony to attack the invader. The members of an ant colony also carry a chemical badge that says to the others "I belong here." Spread a little of that chemical badge on an invader and the sentries will allow it to enter the colony as one of their own. The chemical signals used and understood by ants are obviously programmed into their genes.
The communication systems of all living creatures are programmed to some extent by genes. While genes rule supreme over insect communication, many mammals and birds have some flexibility for learning certain types of signals. Songbirds inherit a fixed genetic template of the songs they will sing as adults, but they must hear the songs of adults during a critical period of development
to sing their songs correctly when they grow up. Some birds, such as cowbirds, can learn the songs of a different species. Cowbirds, known for laying their eggs in the nests of other birds, including golden warblers, are born with a genetic template for their own species' songs, but when raised in the nest of the golden warbler, they learn to sing the songs of their foster parent.
The development period of song learning among birds is similar to the babbling phase of human babies and other young primates, such as the vervet monkeys that live on the African savanna. Vervets are born with a genetic template for specific types of calls, but they must learn to use them in the proper contexts by observing adults. The foundation for human language -- grammar and syntax -- is genetically programmed in humans, but the ability to speak human language must be learned from exposure to adult speech. Many species of animals depend on experience and learning to communicate. The difficult part is figuring out which species need to go to "school" to communicate effectively and which are fully programmed by their genes. Humans are regarded by humans, of course, as the savants of communication. It may seem logical to conclude that the complexity of communication systems follows a hierarchy leading from humans to apes to mammals and birds and on down to insects. But it's not so simple. The most complex system of communication next to that of humans is found in the dance steps of the honeybee.
How can that be? Nature isn't concerned with how an organism communicates as long as it finds a way to do it successfully. The forces that help an organism achieve a successful system for communicating -- whether simple or complex -- are known as natural selection and sexual selection.
Natural selection basically means that nature favors any trait that improves an animal's chances of survival. If screaming a warning or releasing a certain chemical when a predator is sighted helps keep the family or kids from becoming dinner, then nature will favor those signals, which will become established in a species.
Sexual selection is an equally powerful force that shapes an animal's come-hither signals, such as lilting songs and flashy ornaments or displays. Sexual selection favors any signal that helps an animal win at the mating game. Whichever of the sexes is in the driver's seat when it comes to choosing a partner -- usually females, as most scientists now realize -- will have the greatest influence on shaping the signals that the opposite sex uses to woo a partner.
Some scientists argue that sexual selection has been more influential than natural selection in the evolution of communication. Step out onto your back porch on a spring morning or take an evening stroll on a country lane and it is easy to see why. At dawn and dusk, most of the animals and insects that can be heard are chatting about sex. The chirping of crickets, the croaking of bullfrogs, and the repertoires of songbirds are solicitations made by males at the insistence of incredibly critical and demanding female audiences. Likewise, the colorful plumage and exaggerated physical characteristics that many animals display have typically developed to attract members of the opposite sex.
The common definition of communication -- that a sender provides information to a receiver through a signal -- follows an "information model" to interpret the exchange. Some scientists argue that the information model reflects a human-centric bias because information is so highly valued in human society and is conveyed by human language. To understand better what many mammals and birds are experiencing when they communicate, it may be more useful to compare human nonverbal communication with the systems used by animals. From that perspective, communication becomes less about exchanging information per se, and more about managing or manipulating behavior.
In the late 1970s and 1980s, scientists Richard Dawkins and J. R. Krebs popularized the idea that communication is primarily a means of manipulating behavior. According to Dawkins, the bottom line for all species is to pass their genes to the next generation, assuring a type of genetic immortality. So each party in a conversation has its selfish interest at stake, and selfishness is at the root of all behavior. Dawkins later developed the notion of the "selfish gene," which underlies much scientific interpretation of animal behavior and communication today. Not everyone agrees with this interpretation of behavior, but Dawkins and Krebs are so commonly cited in scientific papers published on animal communication that their argument cannot be ignored. Most scientists would agree that communication is indeed motivated by the sender's need or desire to manipulate the behavior of another animal but that the receiver also extracts some key, albeit simple, information from a signal to make a response.
One question that scientists still debate is whether the sender or the receiver has the greater influence on the emergence and refinement of signals. Ornithologist Eugene Morton, of the Smithsonian Migratory Bird Center in Virginia, and Donald Owings, a professor at the University of California at Davis, both argue that the receiver, or "perceiver," as they call it, runs the show. They prefer the word perceiver because it indicates that the listener plays an active role. To describe their perspective on how vocal and visual signals have evolved, Morton uses the analogy of a stand-up comic. For example, Jerry Seinfeld, who is known to drop in unexpectedly at small comedy clubs around New York City to try out new material, drops into a club, delivers some new jokes, closely watches the audience, and sees that the jokes aren't going over well. Only a couple of people are chuckling, probably just because he's Jerry. He switches gears, moves to another set of jokes, and gets a slightly better response. He keeps trying new material until something clicks and he has the audience rolling with laughter. The bad jokes go into the trash and the good ones are kept for his road show. But while Seinfeld may make a hit with his new jokes, who is really in charge? Morton and Owings say it's the audience, because they determine which signals from the stage live or die.
In the animal kingdom, the sender must come up with a signal that gets the attention of the audience -- the receiver -- and elicits the desired response. If it does not, the force of natural selection or sexual selection will ensure that the unsuccessful sender fades from life's stage.
Last night, my group in the Amazon had an opportunity to witness an effective signal from a remarkably talented Peruvian guide, who had taken us on a night hike at another location in the rain forest. An hour into the hike, the guide suddenly thrust out his arms to block anyone from moving ahead and whispered in Spanish with unmistakable urgency, "Alto, alto!" He shone his flashlight in front of us, illuminating a juvenile fer-de-lance pit viper curled on a branch jutting out into the trail. These snakes, among the deadliest in the world, are on average five feet long and deliver about 105 milligrams of venom with a single bite -- only 50 milligrams are needed to kill a person. The viper's bites are a common cause of premature death among people in Central and South America, particularly in the Amazon. Had one of us brushed against it, we would have had one person fewer in our party. The guide's urgent signal communicated danger and altered our behavior. If he had casually said, "Umm, there's a snake," we might not have paid much attention. All of the signals in the animal kingdom have proven effective over time at getting their intended audience's attention.
It is important to note here that a signal does not always require a response. Sometimes the receiver simply is not interested in whatever the sender has to say, no matter how effective the signal may be in other circumstances. Females that are being solicited by males for mating ignore the majority of the signals sent their way. Their lack of response can be interpreted as, "Ho hum. You are not quite what I'm looking for." This lack of response to mating signals certainly holds true for many human males, as well. Unreturned telephone calls and e-mails can be just as informative as a verbal reply such as, "I'd rather not be with you." Relationships with friends or lovers are over when the other person stops responding to calls or e-mails.
Sometimes it simply pays for the receiver to keep quiet. Harold Gouzoules, of Emory University in Atlanta, has studied primate behavior for more than two decades. Chimpanzees form social cliques that possess varying degrees of dominance and status. On any given day in the life of an average male chimpanzee, that male has a good chance of being pushed around or thumped on by a more dominant male, much like middle school for adolescent human primates. The usual response among chimpanzees to a beating is loud screaming, which is intended to solicit help from one's buddies. Sometimes that approach works, but it's not guaranteed. Gouzoules has found that the silent treatment from a chimpanzee's allies when it is being beaten by a more dominant male is a clear signal that says, "Uh, sorry, pal. It's not in my best interest at the moment to help you. If I look the other way I might win points with the big boy." On the other hand, if the male's allies respond to the plea for help and they win the conflict, their social group can boost their status in the community. The popular "reality" television show, Survivor, was nothing more than humans playing chimpanzee politics.
When communication occurs, it must take place through one or more of the animal's senses. Remarkably, nature has been quite conservative in the development of senses in its animal subjects. Although an estimated 10 million species currently reside on the planet, all must make use of five basic senses -- vision, hearing, smell, touch, and, to a lesser degree, taste. The senses provide most animals with at least five basic types of signals to choose from: visual displays, vocal sounds, chemical signals, tactile signals, and sometimes messages sensed through taste. Overall, the environment determines the extent to which a particular sense is developed more than any other, or which senses might be combined in a particularly useful way. The five senses are well developed in humans, but animals possess senses that are often more acute or broader in their range. Some mammals, birds, and insects can hear sounds out of our range of hearing and see colors or patterns that are invisible to the human eye. Depending on the species, the environment, and the influences of natural and sexual selection, some senses will be favored over others. Ants rely most heavily on smell and touch. Moths rely primarily on uncanny olfactory abilities. Elephants can sense vibrations in the ground over long distances through the pads of their feet.
While most signals in the animal kingdom are limited to the five senses, nature has provided for two rather exotic exceptions. Out in the Amazon and in the streams beyond our camp are silvery knife fish that sing the body electric. Electric fields have been adopted as communication tools by a variety of aquatic species, including sharks, eels, and some species of fish, which use them to sense their prey and communicate with members of their own species. Electricity as a medium for signals appears to be limited to creatures that live in the water, which serves as a good conductor of electrical signals. The knife fish generate weak electrical charges to converse, defend territory, locate food, and navigate at night. When males send electric pulses to each other, they are usually saying, "My clump of plant. Find your own." But electrical charges take on an amorous tone between males and females. When knife fish mate, they swim in a spiraling ballet and sing an electric duet that rises and falls in intensity and cadence. Philip Stoddard, a specialist in electrical communication at Florida International University in Miami, recently learned that these couples can adjust the frequency of their electric love songs to keep one of their predators, the electric eel, from eavesdropping and devouring them.
Knife fish range from 3 to 12 inches long and thrive in tropical rivers and lakes. The eel that dines on these fish averages six feet long in size. It swims about attempting to eavesdrop on courting male and female knife fish and on squabbling, territorial males. The eel's sensitivity to the electrical signals of its prey is limited to low frequencies. The knife fish, which began its evolutionary journey with a simple signal at a low frequency, has developed a more complex pulse at frequencies above the eel's sensitivity. Stoddard made the discovery using an electric eel named Sparky and the tape-recorded signals of knife fish in a big tank. He put an electrode in the tank and released a simple signal that the eel could easily detect. The eel assumed it was dinner and responded by swimming to the electrode and blasting it with 300 to 400 volts, as it would to stun its prey. But when the knife fish's complex signals were played in the tank, the eel responded only a third as often, suggesting that the fish have altered their signal over time to avoid being eaten. The experiment also suggests that the eel may be catching on, since it can detect the complex signal a third of the time.
Electricity is a powerful force in a six-foot-long eel: the first time Stoddard conducted the experiment, he did not have his amplifier and sound equipment plugged into a surge protector. When Sparky became excited by the electrode that was mimicking the knife fish and gave it a big jolt, Stoddard's equipment was fried.
The other method of signaling that is unique among animals is known as bioluminescence, which is the ability to generate one's own light. Technically, this falls under the class of chemical signals, but generating light takes a species beyond the typical olfactory signals that account for most chemical communication. Bioluminescence is most widespread among marine animals that live in the deep ocean, although you can get a wink from a bioluminescent creature by standing on the beach at night and watching tiny dinoflagellates fluoresce in the roiling surf. Edie Widder of the Harborview Oceanographic Institution in Fort Pierce, Florida, argues that bioluminescence is the most underappreciated of all modes of communication. She estimates that it is used by 90 percent of all creatures that live in the darkness of the midocean, which ranges from about 500 feet to more than 3,000 feet deep. Sunlight does not penetrate below 500 feet in the ocean, so some animals there have developed their own headlamps and a few other truly bizarre features that employ light. Bioluminescent signals are given to attract mates, lure prey, and frighten potential predators. The deep ocean, which I have been fortunate to visit in the Russian submersible Mir 1, looks a bit like a surreal night sky with jellyfish, lantern fish, and other critters appearing as twinkling and shooting stars.
Of all the residents of the midocean, the anglerfish is among the most peculiar. Ferocious-looking sea monsters with oversized jaws and rows of sharp teeth, these fish have small extensions on their heads that resemble fishing rods with lighted lures, which hang down in front of their mouths. I watched a team of Russian scientists from the P. P. Shirshov Institute of Oceanology catch some of these creatures with fine mesh nets dropped to about 3,000 feet. To my amazement, the horrific anglerfish that came up from the depths was about the same size as my little finger.
On land, chemical olfactory signals play a key role in communicating information about territory and a readiness to mate. The potent smell that tends to get house cats neutered is a chemical signal that the female sprays on rugs and furniture as an invitation for males to mate with her. The ants that form a trail across the kitchen counter are premier biochemical experts, invading in columns after foragers have laid a chemical trial via little puffs of scent from chambers in their hindquarters.
As mate attraction signals, chemicals are used by most species of mammals. In some cases, chemical signals are essential for arousal. The male elephant dips its trunk into a potential female mate's urine to assess whether she is receptive, and then touches the tip of its trunk to an organ inside the roof of its mouth called the vomeronasal organ. If the female is in heat, a chemical in the urine will give the male an instant erection, the elephant version of Viagra. In fact, the female chemical stimulates production of nitric oxide, which is the same potent blood vessel dilator acted on by Viagra. If the female is not in estrus -- the animal version of ovulation -- no signal is received by the male elephant. Schooling fish will release chemical warnings when being attacked by a predator, but chemicals do not diffuse as well in water as they do in air, which is why land mammals use them to a much greater extent.
The ocean is instead a sensual universe of sound because sound waves travel more efficiently than light waves or chemicals through water. The aquatic environment has pressured its inhabitants to become vocal communicators and to develop abilities to hear and locate sounds from great distances. During a brief media fellowship at the Woods Hole Marine Biology Laboratory, I had the opportunity to examine the ear bones of a dolphin that had died after beaching itself. The bones looked nearly identical to those of the human ear except that they were several times larger. Their size reflects the dolphin's successful adaptation to the marine environment.
Dolphins and killer whales use both low-frequency sound waves and high-frequency sound bursts, many of which are out of our range of hearing. Most whale species communicate only with low-frequency sounds. Humpback whales are renowned for their haunting songs, which can travel long distances in the water, but the real long-distance communicators of the sea are finback and blue whales, which are the largest animals on earth, growing to 90 feet in length. The calls of finback and blue whales can be detected thousands of miles away. Like the songs of humpbacks, the vocalizations of finback and blue whales are probably designed to attract mates. Finbacks and blues normally communicate at depths of about 3,000 feet. There they can take advantage of a phenomenon known as the sound fixing and ranging (SOFAR) channel, a layer of the ocean that focuses the whales' low frequency sound waves and allows them to travel the greatest possible distances. The transmission of sound underwater is influenced by temperature, salinity, and pressure, and the conditions at 3,000 feet are such that sound waves become trapped and travel along the SOFAR layer for thousands of miles. The call of a blue whale is considered the loudest of any animal on earth, reaching levels of nearly 190 decibels, which is about as loud as a commercial jet taking off.
In the 1940s a young scientist named Donald Griffin discovered that bats navigate and locate their prey by bouncing high-frequency sound waves off the objects around them and analyzing the different rates of return of the sounds to their little brains. Griffin called this capability echolocation. Humans had developed a similar technology, which we call radar on land, and sonar, under water. At the time of Griffin's discovery, the navy was already using sonar, during World War II, to detect submarines. After the war marine biologists, inspired by Griffin's discovery, borrowed the navy's sonar technology to explore communication in dolphins and whales.
In the mid-1950s, dolphin echolocation was only a theory. Marine Biologist Ken Norris's team figured out a way to blindfold a dolphin and conduct tests to demonstrate that dolphins have sonar. "He did a tremendous amount of work to understand how they do it," said Dr. Daniel P. Costa, a former student of Norris's and a professor of biology at the University of California at Santa Cruz.
Echolocation, which is used by most marine mammals, is not always used for communication. Marine mammals are better known for using echolocation, which sounds like repeated clicks to the human ear, to navigate and hunt. But in more recent years scientists have discovered that both bats and dolphins use their echolocation skills to converse. Marine mammal communication, especially in dolphins, is more complex than anyone had imagined.
On land, both sound and light are the big players in communication. Visual signals are far more important to land animals than sound because of the efficient movement of light waves through the air. Most terrestrial vertebrates have a well-developed repertoire of visual signals, including body language, markings, and flashes of color. Our human senses are limited to a middle range of sound and light frequencies. On the upper portion of the light spectrum is ultraviolet light. On the lower end is infrared light. Visible light falls between the two extremes. Birds can see ultraviolet light. Drab-looking feathers in the visible light range may appear like shimmering prisms to a little sparrow. My favorite snake, the fer-de-lance, a pit viper, can sense other animals' infrared radiation with organs called pits, which are covered with a temperature-sensitive membrane that detects body heat, similar to the way soldiers' night vision goggles work. Based on the amount of heat being generated, the snake can get a pretty good idea of the size of an animal that has come into its range.
Giraffes, elephants, and hippopotamuses are known to produce low-frequency vocal signals below our range of hearing to make long-distance calls. Probably many other species will be discovered to produce low-frequency sounds below our hearing threshold. With bats and dolphins chatting away at frequencies above our range of hearing, and large mammals holding conversations below it, it is obvious that a fair amount of animal communication is taking place beyond our sensory awareness. For at least half of the twentieth century, scientists tended to assume that if they couldn't see it, hear it, or smell it, then it must not exist, but they have since developed technologies that can hear sounds in the silence, see the invisible, and sniff out the tiniest whiffs of otherwise undetectable pheromones. What humans lack in sensory range and acuity, we make up for with our big, energy-guzzling brains -- the neurological equivalents of SUVs.
No fancy technology, however, was needed to give research into animal communication its first really big breakthrough. Charles Darwin's era, the nineteenth century, marked the beginning of the formal study of animal communication. Scientists then focused on visual signals because they could observe them in the field and draw and reproduce them in books and journals for others to see. Darwin tended to discount the vocal signals of animals in his writings largely because he could not record sounds. With the invention of the tape recorder in the 1940s, however, researchers could finally go out into the field, make a recording of animal calls, and study them back in the lab. With the ability to listen to sounds in the lab, scientists could develop theories about their meanings, take the recordings back into the wild, and play them to the animals to observe how they responded. These "playback studies" launched the modern field of animal communication. Affordable lightweight digital video cameras are similarly revolutionizing the study of visual signals. The advance of digital technology has made research on both audio and visual signals incredibly productive. Digital audio and visual signals are much more readily broken down for analysis back at the lab, and digital files are easily transferred between scientists via the Internet.
I wish I had brought a digital tape recorder to record the rain forest's night sounds. Not only would I have had something soothing to listen to at home, I could have conducted a simple study of my own. I could have turned the tape recorder on, logged the time at 12:15 A.M., and marked my location with a handheld global positioning system unit. Back home I could have tried to identify the calls of the species I'd recorded and compared my recording with recordings of known species in the region. One of the world's largest collections of animal sounds can be found at Cornell University's Macaulay Library of Natural Sounds, which animal communication researchers use for this very purpose. (Anyone can log onto the sound library's Web site, http://birds.cornell.edu/Ins/, and listen to animal vocalizations.)
My imaginary recording from the rain forest would be pretty busy, with hundreds of different creatures talking at once. With a machine called a sound spectrograph -- another key breakthrough for communication scientists -- I could break down the sounds into individual frequencies to analyze any vocal signal. The sound spectrograph, which may be more familiar as a machine used for studying speech and hearing disorders and music, consists of a tape recorder/playback unit, a device that scans the tape of your sounds, an electronic filter, and an electronic stylus -- similar in concept to the ones used on old phonograph records. It transfers the analyzed sound information to paper. A spectrographic analysis looks similar to a printout from a heart monitor at a doctor's office or a lie detector, with lines on a sheet of paper that represent time, frequency, and amplitude (loudness) of the sound. Spectrographic analyses of the sounds of different species, and comparisons made between species, reveal some rather surprising similarities that I will discuss in detail in another chapter.
Katy Payne, a respected elephant behavior and communication expert from Cornell, demonstrated the power of sound spectrography in the early 1980s. She was visiting a zoo in Portland, Oregon, where two elephants had been separated from each other. Although the elephants couldn't see each other, they could still communicate. Payne said she happened to be standing near one of the elephants when she felt a strong vibration in her chest, similar to what one would experience standing near a pipe organ being played in a church. Payne recognized that the vibrations she felt were the result of low-frequency sound waves. She made recordings of the silent vibrations the next time she visited the elephants and demonstrated with the sound spectrograph that the elephants were communicating via low-frequency sounds. The findings launched a new field of study in elephant communication.
Payne was familiar with low-frequency sounds, which travel the longest distances of any frequency, from her studies in the 1970s of humpback whales and their long-distance calls. Her former husband, Roger Payne, is known for discovering that humpback whale vocalizations are actually songs. After she published her paper on elephant sounds, Payne collaborated with Joyce Pool and Cynthia Moss, who were already studying elephant behavior at the Amboseli National Park in southern Kenya. Together, they discovered much of what is known today about the meaning of elephant vocal signals.
One of the more novel inventions for studying animal communication comes from the laboratory of Peter Tyack at the Woods Hole Oceanographic Institute, in Massachusetts. Tyack and his students have invented an underwater microphone that can be attached to the heads of marine mammals with a suction cup. With this minimally invasive device, Tyack is collecting an enormous amount of data on vocal signals from marine mammals, including endangered right whales. The recordings of clicks and squeals made by these remarkable creatures sound like something a Hollywood special effects team might conjure for a space alien, and they are expected to yield important new insights into the behavior of right whales, which might enable scientists to reduce the number of collisions that occur every year between these whales and boats. Another of Tyack's inventions, which lights up when an animal is vocalizing, can be attached to the heads of dolphins for studies of dolphin interactions in captivity.
Animals do not need any special equipment to be expert sound and light engineers. They are natural physicists that exploit light and sound in sophisticated ways. To keep up, animal communication experts must learn the science of light and sound, how they are propagated and received, before they go out into the field to begin recording and filming their subjects.
Scientists have discovered that animals are experts at exploiting weather conditions and the physical conditions of their environments so that they are heard or not heard, and seen or not seen. The species living here in the rain forest of Peru must engineer their calls to accommodate all of the obstacles, such as leaf cover, that can deflect and degrade the sounds intended for a potential receiver. Overall, short, loud bursts of sound tend to be more effective than longer calls at cutting through the dense foliage.
There is no natural environment on earth noisier than a virgin rain forest. Every species here has developed clever or remarkably sophisticated strategies to ensure that its voice is heard. The noise creates a real challenge for the smaller residents, such as male tree crickets, which need to get the attention of females, often from a relatively long distance. Some species of crickets maximize the volume of their stridulating calls by chewing a hole in the middle of a leaf to create a sound baffle, in the same manner humans build a stereo speaker. The leaf functions as a speaker cabinet, with the cricket in the center acting as the speaker.
A species of tree frog in Borneo has a unique approach to getting its mating call heard over the din. Metaphrenella sudana, which is only an inch long, has learned to exploit the sound properties of a water-filled hole in a tree in the same way that a person uses resonance in the shower to sing like a star. The frog searches for a suitable hole and then partially submerges itself in the water. Its forte is the ability to adjust the frequency of its call to the size of the hole and play the tree like a musical instrument. As it sits in the hole, it begins vocalizing at different frequencies -- lo lo lo, la la la, le le le -- until it hits the one note that makes the hole and tree resonate.
The time of day affects how sound travels in any environment, and this fact is not lost on animals and insects. Early morning and late evening produce conditions that allow sound to travel greater distances than during the middle parts of the day. Sound travels best at night, which is why the rain forest is so wonderfully noisy between dusk and dawn. For species that sleep at night, dusk and dawn are their windows of opportunity to get the best resonance and distance out of a signal. This is why animals, especially birds, tend be more active and noisy in the early morning and late evening. The British call the phenomenon of birds singing in the early morning the dawn chorus. Because of the superior sound conditions, dusk and dawn are the times to conduct the serious business of attracting mates and defending territory. For predators, it is the best time to eavesdrop on conversations and track down their chatty prey.
Another way animals and insects ensure that their calls connect with the intended receivers is by developing their own specialized frequencies, which are determined primarily by the size of their bodies. Recently, a scientist visiting near this region of the rain forest made an audiotape of a little of the night's music. When he took the tape back to his lab and analyzed it, he discovered that this seemingly chaotic banquet of sound is actually highly ordered. Each animal and insect is tuned to and calling on its own species-specific frequency, in the same way that radio stations use different signals so that many stations can be on the air at the same time. You might say that the crickets are playing on WCHIRP FM 102, while the tree frogs are at WCROAK FM 97.1. Mosquitoes, which really bug me, buzz at a perfect high C.
Bernard Krause, a professor at the University of Oregon in Eugene, has found that in older tropical rain forests some species, such as the Asian paradise flycatcher, have become so specialized that their voices occupy several niches of the sound spectrum at the same time, "thus laying territorial claim to several audio channels." His recordings from undisturbed rain forests around the world demonstrate a remarkable stability in the combined voices of the residents from year to year. The stability of the ambient sound gives each region a unique sound signature, or fingerprint.
"Over a number of years we would return to the same sites," Krause says, "only to find, when the recordings were analyzed, that each place showed incredible bioacoustic consistency, much like we would expect to find from fingerprint matching. The bird, mammal, and frog vocalizations we recorded all seemed to fit neatly into their respective niches. And the bioacoustic niches from the same locations all remained the same given the time of year, day, and weather patterns. Having just begun to work in Indonesian rain forests, early analysis indicates similar results from each of the biomes we have visited and recorded."
Krause compares the sounds of the nighttime jungle to the music of a symphony orchestra. Different instruments are tuned and played at specially timed intervals to avoid drowning each other out. Animals do the same thing by finding their niche frequencies and taking advantage of the pauses that others make during their calls. Even though the sounds seem chaotic to the uninitiated human ear, all of the vocalizations are actually highly choreographed. Of course no rain-forest conductor coordinates the thousands of voices booming in the night. The orchestration of the voices of thousands of animals and insects calling together developed over time, as each species fine-tuned its signals and reception for maximum efficiency.
According to Krause, the Jivaro and other tribes of the Amazon Basin have known this information all along. These indigenous people are expert at identifying the sounds of individual animals as well as subtle differences between various mini-habitats in a region. Moving as little as 30 feet in one direction in an old-growth forest will reveal an entirely different ambient sound signature. The local tribes are able to travel at night in total darkness and identify their location solely by the sound. Krause believes that ancient humans would have possessed the same intimate knowledge and familiarity with their environment. His research suggests that the roots of musical composition can be found in the animal orchestras of the old-growth rain forests.
Comparisons of the vocalizations of songbirds to music are not meant as a metaphor. Birdsong is music. It is supposed to sound pretty. The emotion that birdsong evokes in a human listener is not far from the physiological response it is intended to evoke in the female receiver. Of course, female receivers are evaluating the songs for much more than just their nice sound. They are judging the quality of the songs and the repertoire, which scientists believe reveals information about the quality of the singer's genes. (Some female human concertgoers also evaluate rock singers' jeans and determine their own willingness to mate based on the quality of the songs and repertoire.)
Why did animal communication first arise? The prevailing theory, credited to the classical ethologist Niko Tinbergen, is that animal communication evolved as a more economical substitute for physical violence. If animals can growl and posture and bluff instead of hurting each other and still get what they want, then why get hurt? Injuries from fighting make it harder for an animal to conduct its business of mating, defending territory, and finding dinner. Life in the wild is risky enough as it is. Violence is very expensive in nature's economy, and this is why animals rarely come to blows. Any successful strategy that avoids violence will be favored through natural selection. The injured hotheads will die off while the successful bluffers mate and pass along their genes.
Tinbergen and Konrad Lorenz developed the concept of "intention movements" to explain the evolution of communication, suggesting that the signals an animal uses to communicate in a conflict arose from the same physical movements and vocal sounds that it would normally use during an actual fight. For example, many mammals reflexively retract their lips when fighting to protect them from being bitten off by an opponent, and they retract their lips when biting another animal. That reflex has evolved into baring one's teeth at a potential opponent. (The human snarl curls the lip to reveal a canine tooth, which was larger in our ancient ancestors.) During a conflict, the natural fear and aggression an animal feels will cause its hair, assuming it's a hairy beast, to stand on end. This autonomic, or involuntary, response to fear and aggression, called piloerection, has become another bluffing signal in a conflict -- it makes the animal look bigger. The idea is that if an animal appears as if it intends to fight by assuming the various postures and vocalizations associated with fighting, maybe the opponent will back down.
I will present all of these modes of communication in greater detail in later chapters. In the meantime, as I prepare to slip away from camp, the sounds are particularly intoxicating. But it is February and the mosquitoes at this time are abundant. Outside the protective netting of my hammock, these miniature vampires quickly engulf my head like a thick cloud, filling my ears with their high-pitched, annoying "bzzzzzr, bzzzzzr." Rain-forest veterans warned me about them, but I had no idea there would be so many at all hours of the day. Mosquitoes have short lives, so I suppose they must make the best of it, but I feel as if I've been tricked. In all of the Tarzan movies I saw as a kid, never once did the king of the jungle slap a blood-engorged mosquito off his neck and curse. I have lathered so much Deet insecticide onto my skin that I can smell the stuff on my breath. Even so, my ears, which protrude from my head like satellite dishes, are already burning and itching. With a shudder and a repressed desire to slap the sides of my head, I sling a light pack over my shoulder, tuck my pant legs into my boots, and slip out into the night for the party. A mere 20 feet from the edge of the camp's platform, the clearing yields to the forest. I can barely see what appears to be a dark hole that might be the trail leading to the canopy walkway about half a mile away.
My heart pounds faster as I move into the near total darkness of the surrounding jungle. Feeling like Alice stepping through the looking glass, I stumble blindly in the dark along a muddy trail until I am at a safe distance from camp. Finally I turn on my rubber-coated flashlight to illuminate the narrow path, no more than a couple of feet wide. A sense of marvel and the distinct tingle of fear sweep through me as I head deeper into the jungle. The scientists did not caution us to stick close to camp for nothing. Fer-de-lance could be anywhere, and I have to be careful not to brush against branches or step on something long and slender that is waiting for small prey to come along. After last night's encounter with the viper I admit developing something of a preoccupation with this cousin of the bushmaster and rattlesnake. Brown, sometimes gray, with light stripes and diamond markings similar to those of rattlesnakes, the fer-de-lance has a distinctive yellow throat and jaw, which communicate a simple message: "I'm poisonous. Don't try to eat me."
In nature, colors are very simple codes with specific, universal meanings. Yellow and red (and sometimes orange) are the animal kingdom's favored colors for advertising that a particular snake, insect, frog, bird, or other critter is venomous or at least not very tasty. I especially do not want my flashlight to pick out the yellow throat and open mouth of a fer-de-lance that has raised itself up from the ground in a taut S-shape. That would mean I -- a large primate and potential predator -- have frightened the poor fellow and made it ready to defend itself. Given that communication arose as a substitute for violence, the snake will try to warn me before using up its valuable venom -- if I see it. As a city dweller, I am at a distinct disadvantage in the jungle at night. Most of the animals, including the tree frogs and crickets, can see me, hear me, smell me, or feel the vibrations of my feet on the path long before I am aware of them.
If I possessed infrared sensors, I would be able to see the many creatures that are certainly watching me. I decide to turn the flashlight off and stand in the darkness for a few minutes to soak up the sounds and get a feeling for how my own inferior senses work in this unfamiliar environment. My sense of touch tells me that the mosquitoes are continuing to attack my face, but my eyes can just make out the shapes of trees and undergrowth although not much else because the thick canopy blocks the moonlight. Sound is about the only thing my senses can pick up, and it is overwhelming since I cannot distinguish the different animal sounds with anything near the skill of the Jivaro.
After ten long minutes in the darkness I flick the flashlight back on and continue my illicit walk down the narrow trail. The flashlight restores my human vision and confidence. The moment I light up the trail, hundreds of flying insects are attracted to the jiggling beam. Quite a few theories have been developed about why insects, especially moths, are attracted to light. Some scientists say it's because they use the moon to navigate and confuse the brighter rays of a porch light or flashlight with their lunar guide. Curiously, the same phenomenon occurs in the ocean. During a night scuba dive, tiny copepods -- basically the bugs of the sea -- swarm around a flashlight just like these insects. Copepods migrate toward the surface with the first light of day, and their sensors confuse the flashlight with the sun. Here on the trail, my flashlight beam creates an opportunity for bats that quickly zero in on the halo of bugs. I fancy I can almost hear their high-pitched sonar as they ping the bugs and dart in for an easy meal.
The calls of several douroucouli, a very vocal nocturnal monkey, pierce unexpectedly through the upper canopy. The douroucouli are tiny primates with big eyes, specialized for night vision, that have earned them the nickname of owl monkey, the only species of monkey known to be active at night. Their call sounds like a high-pitched "wook wook" and carries a distinctive sense of urgency -- the douroucouli's alarm call. Most species of primates regard their human cousins as predators, and these guys are definitely alerting each other to my presence on the trail. I don't know whether they heard me, smelled me, or saw the flashlight first. Either way I feel guilty for upsetting them. Local people hunt them for food and sell their fur. The monkeys are also captured and sold as pets and for use by pharmaceutical companies. The group of monkeys I have alarmed is most likely a family. Males and females mate for life and generally have two to five youngsters at any given time sponging off Mom and Dad at home. Dads carry the little ones on their backs and take responsibility for most of the childcare. These monkeys are extremely territorial and mark their boundaries by means of a gland at the base of the tail that excretes an oily brown liquid. Owl monkeys make about 50 different calls. They squeak, hiss, bark, hoot, and meow, and all the calls have quite specific meanings, including alerting each other to a food cache, rallying together, and bonding.
Alarm calls are especially common in primates. Captive monkeys used for experiments at medical labs quickly adapt their alarm calls to veterinarians and technicians who perform invasive procedures. The monkeys can make a disturbing fuss on the days that blood must be drawn or when one of them is removed and taken to surgery. Whenever a stranger shows up in their midst they go absolutely bonkers with angst because they have no idea what to expect and tend to associate unfamiliar humans with pain. Their cries of fear are unmistakably anguished and can provoke sorrowful emotions in empathetic lab workers and students unaccustomed to such calls. Of all the sounds in the animal kingdom, it is the cries of primates that I find the most disturbing. But closer to home, as the West Nile virus spread from crows to squirrels, people in Illinois began reporting sounds like a baby crying in pain. It turned out to be squirrels that were infected with the virus and experiencing neurological degeneration.
I move on toward the walkway and startle other animals as my boots squish into the muddy trail. Crickets, toads, and tree frogs abruptly cease their calls as they sense my approach, but resume their business of courtship and territory defense as soon as I pass by. Tree frogs make up a large section of tonight's orchestra. I amuse myself with a little game of stop and go -- silencing the crickets and frogs, then waiting for them to start in again. Funny how one can sit in an apartment in a city surrounded by marvels of man-made communication technology -- telephones, faxes, cable television, music CDs, and high-speed Internet -- and be bored to tears. It is much more fun to interact with the frogs.
After about a half-hour walk, I reach my destination at the end of the trail. Stretching overhead is a maze of steel cables, ladders, and webbed rope bridges that ascend to the top of the canopy. I climb a sturdy ladder through the first layers of growth to a small platform that leads to a series of rope bridges and more ladders. A green tree snake slithers over a limb and out of sight, startled by my sudden appearance. I am reminded not to lean against branches or tree trunks and to make sure I can see where I'm placing my hands. The mosquitoes mercifully thin out with the altitude, and moonlight begins to break through the thick foliage as I approach the platform at the summit. The top consists of a bridge, constructed of rope webbing for sides and an aluminum bottom, which spans about 30 feet between two trees.
At last, the unbroken rain forest stretches before me to the horizon in every direction. Seeing it is a profound and moving experience. The humid, floral-scented air vibrates wildly with the primal chorus of exotic tropical screech owls, lyre-tailed nightjars, short-nosed tree rats, kinkajou, douroucouli, cicadas, and probably a few creatures still unknown to man. The night is thrillingly alive and stares back with glowing orange eyes from the limbs of giant mahogany trees, acacias, and thorny palms. Here, standing at the top of this stairway to heaven under a brilliant three-quarter moon, one can hear the unbridled voices of nature and glimpse a vision of a primordial planet from some distant epoch teeming with strange and wondrous varieties of life. Hearing so many different voices is like stepping out of New York City's Penn Station for the first time and being bombarded with shouts in Spanish, Hindi, and Vietnamese, honking taxis, strange smells, sexually enticing billboards, and blazing neon signs. The seemingly chaotic sounds of the jungle remind me of the biblical story of the Tower of Babel.
A metaphor in discussions about the origin of language, this story in Genesis recounts how people have gathered from the wilderness to create a new city after the great flood that destroyed civilization. They build a tower that reaches to the heavens to "make a name for themselves" so they will never be dispersed again. God does not like their plan, so he destroys the city, scatters everyone to the far ends of the earth, and makes them speak different languages.
The opening sentence of this biblical legend refers to the period before the people came from the wilderness and started building the city of Babel and their own stairway to heaven. As I stood on the canopy walkway surrounded by the voices of nature, the sentence began to make sense in a rather odd way:
"Now the whole earth had one language and few words."
The ancient Greeks referred to animal vocal sounds as the natural language. Might this wonderful and tightly choreographed orchestra of voices in the rain forest represent a single language that all the species understand? Perhaps monkeys and birds understand each other. If this is true, how could it be? Clearly, different species make distinctly different vocalizations, but they also share the same five senses to a large extent and have similar needs. Those that live together in the same environments had to deal with the same physical properties of light and sound when developing their signals over the ages. Similar environmental conditions would tend to cause vocal signals to bear at least some similarities in their structure, and it turns out from comparisons of sound spectrographs of different species' calls that this is true. For reasons you will see as we move along, the forces of natural and sexual selection have driven the communication of widely divergent species down similar paths.
Consider human language. No matter what region of the world in which we might have been raised, and no matter what types of words we use to describe the things around us -- German, Russian, English, or Japanese -- we all speak a human language and follow the same rules of grammar and syntax. We might not understand the words that another person is speaking, but we can usually determine whether that person is hostile or friendly or upset, and by using gestures and various emotional expressions, we can often get the essence of what that person wants. Animals of different species sound different as well. Dogs bark, birds chirp, and horses whinny, but they are astute at understanding each other. Animal communication is not as complex as human language because there is less information to be conveyed in an animal's daily life. But humans and animals alike, regardless of race or species, talk about the same things every day -- that is, sex, real estate, who's boss, and what's for dinner.
The whole earth does have one language with few words, and all species, including humans, continue to use it every day. It is a natural language that stems from the evolutionary roots shared by each of the 10 million species that inhabit the planet. We may see ourselves as quite separate from the animal world, but as we move along I hope to show that we still have a seat in the orchestra.
Copyright © 2004 by Tim Friend
Breaking the Codes of Animal Language
Breaking the Codes of Animal Language
"No matter what species," writes acclaimed science journalist Tim Friend, "we're all concerned with the same topics of conversation -- sex, real estate, who's boss, and what's for dinner." In Animal Talk, Friend draws upon years of field research, interviews with preeminent scientists, and lively personal anecdotes to find out how our animal neighbors communicate and what their languages mean. From bird calls to whale songs, laughing hyenas to rattling snakes, an elephant cry in the jungle to the bark of a Chihuahua in his own backyard, Friend tells the grand story of animal communication through the sounds, stripes, scents, and signals of the animals themselves.