Animal Communications

Animal Communication

by Jack W. Bradbury, Sandra L. Vehrencamp

Senders and receivers

An animal that provides a signal is called a sender. The animal to which the signal is directed is the receiver. The receiver uses the signal information to help make a decision. For example, if a receiver must choose either to fight with or to flee from an opponent, it brings to this decision biases and thresholds passed on to it by successful prior generations. This information helps the receiver avoid harm and find food, shelter, and mates. Prior experience in the receiver’s own life may also play a role in shaping its evaluation of the situation. If it has routinely lost fights to larger animals, a useful strategy would be to assess the size of the opponent. This may be done by using vision or other means. For example, in some cases an opponent broadcasts a low-frequency sound signal at the receiver. Because only large animals can produce low-frequency sounds, this signal provides evidence that the opponent is large. The receiver integrates its perception of the sound frequency with its prior experience and inherited avoidance of harmful situations and thus decides to flee.

In this example, the receiver can interpret the signal only if it understands that low-frequency sounds tend to be associated with large body sizes. The association between alternative signals (e.g., sounds of different frequencies) and different alternative circumstances (e.g., relative sizes of opponents) is called a code. Codes can be characterized as probabilities that a sender will emit a given signal in any given circumstance. In a perfect code, only one signal will be used in a given context, and only one context will evoke that signal. Real codes do not need to be perfect, but they do need to be good enough that a receiver attending to signals makes better decisions than if it ignored the signals and relied only on other sources of information.

Animals differ widely in the mechanisms by which they acquire signal codes. Some codes are inherited genetically. For example, the sound-producing structures of many male insects generate a limited range of sound frequencies, and the ears of females are pretuned to be most sensitive to those frequencies. In other species, senders’ sounds or body odours are determined by random genetic processes, and receivers must learn which signals go with which individuals. Many songbirds have genetic limits on the range of sounds they can sing, but they can learn one or more local variants within those limits during a short period in their youth. In certain species, such as parrots or humans, both sender and receiver must learn the appropriate vocal coding, and they can continue to learn alternative coding systems throughout life.

Different contexts require different kinds of information and thus different signals. The number of signals in a species’ repertoire can range from 5 or 6 in the simplest nonsocial animals to 10–20 in social insects, such as bees and ants, or to 30–40 in social vertebrates, such as wolves and primates. Most animals produce signals to attract mates and then produce additional signals to synchronize mating. Signals for mediating conflicts, including signals of aggressive intention and signals of submission, are also widespread. In addition, territorial species require signals for declaring territory ownership, and in situations in which adults guard or feed their young, both parents and offspring require signals to coordinate parental care. Social animals may use signals to coordinate group movements, to assemble dispersed group members, or to display social affiliations. Some animals have special signals that they use to share food finds, to alert others about predator attacks, and even to alert approaching predators that they have been detected. In addition, bats, oilbirds, porpoises, and electric fish use the differences between their own emitted and subsequently received signals to extract information about the ambient environment. In many of these contexts, the relevant animal signals are designed to provide a receiver with ancillary information about the identity, sex, social affiliation, and location of the sender.

Signal production

The challenge faced by a sender is the creation of a controlled perturbation of the environment that can be detected and recognized by a receiver. Sound production is one mechanism. Sound travels in waves, and thus any sound can be characterized by its component frequencies and the physical size of each wave component (called the wavelength). The wavelength of a sound depends upon its frequency and the speed of sound in the propagating medium. The speed of sound is greatest in solids, intermediate in water, and least in air. Thus, a given frequency of sound in water has a wavelength 4.5 times longer than the same frequency in air, and the same frequency in a solid can be up to 15 times longer than that in air. This is important to animals using sound communication because it is physically difficult for an animal to produce a loud sound with a wavelength much larger than itself. For this reason, small animals tend to communicate with high-frequency sounds, and only large animals use low-frequency sound signals. Aquatic animals require higher-frequency signals than do similarly sized terrestrial animals.

The lowest frequencies that small insects, frogs, and birds can produce as signals may be many thousands of waves per second. Animal muscles cannot twitch this quickly, which makes sound production challenging. One solution is to use frequency multiplication. For example, hard-bodied animals drag a comblike structure over a sharp edge. A single muscle contraction causes the sharp edge to hit successive teeth in the comb, thereby producing a sequence of sound waves. This is called stridulation. Arthropods all have hard exoskeletons, and by mounting the comb on one external body part and the sharp edge on the other, they can stridulate by rubbing the two hard parts together. For example, lobsters rub an antenna against the head, beetles rub a leg against the body, and crickets and katydids rub one wing over another. There are other techniques for frequency multiplication. Terrestrial vertebrates use muscles to force air into and out of their lungs while breathing. If thin membranes are inserted into this airflow, the membranes will flutter, producing sound waves at much higher frequencies than the airflow cycle. This is how frogs croak, lions roar, and birds sing.

To be able to use different sound signals in different contexts, animals must have some way to control and vary the sounds that they produce. Varying the rhythm of insect stridulation or bird breathing is one way to produce different signals. Air-breathing vertebrates can also change the tension on the vibrating membranes to produce quite complicated frequency modulations. A third mechanism is to produce sounds that initially contain many different frequencies and then selectively filter out some frequencies and amplify others. Animals such as katydids, frogs, bats, and howler monkeys have special resonating structures attached to their sound-producing organs that select the radiated frequencies and couple the sounds to the medium.

Light is another modality used for producing signals. Most visual signals rely on the presence of ambient light that is generated by the Sun. Similar to sound, light propagates as waves. When white light—which contains many different light frequencies—strikes an object, some of it is reflected, and it is this reflected light that creates a visual image of the object. If the object absorbs some frequencies of white light and reflects others, the receiver will see the object as coloured. When red light frequencies are absorbed, the object appears green or blue. When the green light frequencies are absorbed, the colour appears purple. Different animal groups tend to have different ranges of light frequencies that they can see. Birds, lizards, and some insects can see light frequencies well into the short-waved ultraviolet. Humans cannot see these short waves. Thus, in humans, objects that appear to be similar or uncoloured may be seen as different or highly coloured by a bird or a honeybee.

The challenge for a sender is to produce a visible image that is detectable against the background by a receiver. One way to do this is to move the signal body part in front of a static background or to move it in a different direction relative to a moving background. This simply requires normal muscle movements—no additional structure is needed. However, many senders enlarge or decorate the moved body part to increase the chances that the receiver will notice the signal. The sender may also select a site in which to produce the signal that has a simpler background or that is moving in a very different way.

Another major way to catch a receiver’s visual attention is by increasing the contrast between a signal body part and the background. Black-and-white patterns are a common solution. The black is generated by using one of several synthesizable proteins called melanins. White is created by inserting small crystals or bubbles into the organ surface. They are large enough that they scatter all light wavelengths, creating white stimuli. Colours other than black and white are more difficult to produce. Although animals cannot synthesize carotenoid pigments, they can sequester the pigments by eating certain plant parts or by eating other animals that ingest those plants. Carotenoids are relatively stable compounds, generating colours in the yellow-to-red range. There are few natural pigments that are blue or green that animals can utilize for coloration. One exception is the chemical combination of carotenoids and proteins used by arthropods to colour their carapaces (hard outer coverings) dark green or blue. Crabs and lobsters turn red when cooked because the pigment proteins are denatured with heat, releasing the carotenoids. Other animal groups use nonpigment techniques to produce blue or green coloration. One method uses a checkerboard matrix of alternating more-dense and less-dense materials in an external surface layer to selectively scatter certain wavelengths. The colour reflected depends on the size and spacing of the matrix. This mechanism is responsible for producing the blue and green feathers of jays and parrots, the blue skin on the heads of turkeys and male mandrills, and blue eyes in humans and snow leopards. Another technique is to use two thin layers of reflecting material on external surfaces. If the layers have the correct thickness, certain wavelengths are reflected by the two layers out of phase (the crest of one wave coincides with the valley of a second wave), thereby canceling each other out. The remaining light waves are in phase (the crests of the light waves coincide) and are visible as intense colours. Which light waves are canceled depends on the viewing angle of the receiver. Thus, the apparent colour can change as the sender shifts its position relative to the receiver. These are the iridescent colours seen in many hummingbirds and butterflies.

While it is often assumed that ambient light is white, every local environment is actually bathed in its own particular mixture of light frequencies. On a forest floor there may be only small amounts of red and blue light in the ambient mixture because green-reflecting plants absorb both red and blue light strongly. Fine particles in the atmosphere and the dense molecules in water both scatter the shorter blue and ultraviolet light frequencies but transmit the longer red and orange frequencies. The mixture of ambient-light frequencies can be a strong selective force favouring certain colours for signals. Where there is little ambient light, an animal may have to produce its own light (bioluminescence). This ability has evolved in fireflies, ostracod crustaceans (mussel shrimps), deep-sea squid, and marine fish, all of which produce their own light chemically or harbor luminescent symbionts that can produce light for them.

A third major modality used by most animals (with the exception of many birds) is olfactory signaling. Senders deposit or release chemicals called pheromones that receivers later detect by smell or taste. The cost to senders of chemical communication can be minimal, as when feces or urine is used as a signal, or can be substantial, as when complex organic molecules must be synthesized solely for the purpose. Ants are prolific users of chemical communication. Their small bodies contain up to a dozen separate glands, each producing a different chemical compound or mixture of compounds that serves a different social function. Ants use chemical signals to mark their foraging trails, to recruit group members for defense against invaders, to attract mates, to regulate development of different worker castes, to solicit food, and to distinguish colony members from nonmembers. Many mammalian species employ chemical communication for important social functions, such as mate attraction, synchronization of mating, and territory defense. Mammalian glands often produce specialized chemical products, but some species mix various natural body products into a pouch and let bacteria do the work of producing the final pheromone product.

The potential for signal diversity is extremely high in chemical communication, as is the opportunity to create a signal that is very different from background odours. However, this diversity is often constrained by the degree to which chemical signals are appropriately volatile in air or soluble in water, resistant to degradation after release, and detectable by receivers. Animals often limit the volatility or solubility of pheromones by embedding them in an inert carrier compound that releases odorant slowly. This technique is particularly useful for territorial defense. Desert iguanas carry this one step farther by using a carrier that does not release odorant until another lizard flicks the carrier with its wet tongue. The small packets of deposited pheromone absorb ultraviolet light and thus appear as black specks to animals that can see in the ultraviolet spectrum, such as iguanas. Iguanas approach the specks and taste them, thereby releasing the pheromones. Other animals accelerate the dispersal of relatively nonvolatile scents by spreading them over a tuft of fine hairs, actively spraying them into a medium (e.g., air or water), or releasing them into strongly flowing wind or water currents.

Tactile signals involve special patterns of touching, generating persistent eddies in a medium, or the transmission of vibrations through a substrate. Touching during aggressive encounters may provide information about the body size and strength of opponents. The grooming of another individual, called allopreening or allogrooming, has both hygienic and signal functions in many birds and mammals. Courtship signals may include a tactile component for synchronizing mating or gamete release. Roosting with body contact not only preserves heat but also appears to signal pair or group affiliations in mammals and birds. Arthropods make wide use of tactile, eddy, and substrate signals. For example, aquatic male copepods can identify the distinct eddies left by swimming females and track them for mating. The dances of honeybees are usually performed in a dark hive, and attending workers monitor the dancer with their antennae; some signal vibrations may also pass through the honeycomb substrate. Other arthropods attending to substrate-borne vibrations include water striders (using the surface of water), spiders (using their webs), and leafhoppers (using their host-plant stems and leaves).

Electrical discharges can also be used for signals. Two orders of freshwater fish, the Mormyriformes of Africa and the Gymnotiformes of the neotropics, are nocturnal or live in muddy water. These fish create an electric field and use distortions induced by nearby objects to navigate and find food. Not surprisingly, they also use the same electrical discharges to communicate with each other. In both groups, special bioelectric organs have evolved to produce rapid trains of discharges. The waveforms of these discharges vary with species and even with sex, and the rates of discharge can be modulated in complex ways to mediate social interactions. Because of the high resistance of fresh water and the low voltages the fish produce, electrical communication is limited to a distance of about 1 metre (3.3 feet).

Signal transmission

All animal signals degrade as they propagate between sender and receiver. The farther apart the two parties, the greater this degradation will be and the less a signal will stand out from background noise. Senders can do little to reduce degradation once the signals have left the sender. However, they do have a choice of what kind of signal they produce, and evolution has often favoured choices that minimize degradation.

Sound signals transmit efficiently over large distances, around obstacles such as trees and foliage, and in dark environments. Nevertheless, sounds of all frequencies become less intense as they radiate away from a source. Higher frequencies suffer additional attenuation owing to heat losses and scattering of the sounds. Since small animals can produce only high frequencies (short wavelengths), their sound communication is often limited to short distances. Furthermore, ambient sound is often greatest at low and high frequencies, making intermediate frequencies the ones least likely to be obscured by the background.

Propagation of sound is complicated when the sender and receiver are close to a boundary (e.g., the ground for terrestrial animals and the water’s surface for aquatic animals). This is because sound can travel to a receiver by two routes: a direct route along the line connecting sender and receiver, and an indirect route in which the sound bounces off the boundary and up to the receiver. If the two replicates of the sound signal arrive at the receiver out of phase, they will cancel each other out. The closer both parties are to the surface, the more acute the cancellation. Low frequencies are most susceptible to these effects. However, for terrestrial animals, very low frequencies can propagate by a third route, called a ground wave, if the surface is sufficiently porous. Intermediate frequencies, however, are still canceled out even when the ground is porous. As a result, intermediately sized animals that cannot produce low-frequency sounds often climb or fly to locations high above the ground before vocalizing. Elephants, which cannot fly or climb, resort to sufficiently low frequencies that they can be detected several kilometres away. Whales also produce low frequencies and move sufficiently far beneath the ocean surface before vocalizing, which enables their signals to be heard hundreds of kilometres away.

The optimal temporal patterning for sound signals also varies with habitat. Rapid temporal patterns quickly become unrecognizable owing to echoes in heavily forested habitats. In contrast, sounds propagating in open grasslands suffer little from echoes but instead acquire slow artifactual modulations because of air turbulence. Birds, even of the same species, are much more likely to use rapid temporal modulations of their calls, such as trills and buzzes, when they live in grasslands than when they live in forests. Forest birds typically produce long whistlelike notes with slow, if any, modulations.

Light signals also suffer transmission losses. Intervening obstacles such as foliage easily block the straight-line propagation of visual signals, and increasingly distant senders occupy a decreasing part of a receiver’s visual field. Light waves are also subject to filtering and scatter that can distort a signal pattern and decrease its contrast with the background. All of these effects make detection and recognition of a visual signal more difficult at a distance. In addition, reflected light signals require some source of ambient light, and visual communication thus becomes more difficult to achieve at night and in very dark environments. Bioluminescence is, of course, one solution to this problem.

Olfactory signaling differs from sound and light communication in significant ways. Pheromones spread from a source by diffusion and medium turbulence. This process is much slower than the propagation of light or sound signals, and its erratic path can make it difficult for a receiver to locate an odorant source. Whereas sound and light largely retain their temporal patterning as they propagate, temporal patterning of pheromone release is quickly lost because of turbulence. The slow speed, the limited ability to be located, and the loss of temporal pattern constrain the uses of olfactory communication to short-range signals and to recurrent functions, such as territory defense and mate attraction.

The unpredictable effects of turbulence also limit the range over which an olfactory signal can be detected. Receiver moths get around this constraint by sampling wind direction and flying into the wind to trace the chemical source (a process called anemotaxis). Many nocturnal mammals deposit scent marks at multiple locations within their territories. Although no single scent mark is detectable at a distance, the ensemble ensures that any intruder is aware of the owner’s presence in the territory. Some insects and marine species actively seek out sites where air or water currents can convey olfactory signals over long distances.

Signal degradation during propagation is not always a detriment. Many birds use degradation of songs to estimate the distance to competitors. As long as there is sufficient degradation, a territory owner can conclude that the other singers are too distant to be threatening. Many social insects use olfactory signals to mark feeding trails, to give alarms, or to identify colony mates. To avoid confusion and focus attention on a specific location or individual, it is best if these signals have only limited ranges of detection.

Regardless of the modality used, senders communicating with distant receivers face a number of competing influences. Body size, habitat type, time of day, proximity to a surface, and speed with which a receiver must respond all affect the form of the optimal signal. Because species differ in these factors, optimal signals differ between species even when communicating the same information. The constraints imposed by the physics of signal production and transmission account for an important fraction of the diversity seen in animal signals.

Signal reception

The receiver’s task is to detect signals against the background and to discriminate between different signals. Most animals use the same sense organs (eyes, ears, noses, touch receptors, etc.) for signals that they use to detect other external stimuli. Their brains also process all sensory stimuli, both signals and nonsignals, with similar procedures. However, communication is sufficiently important that most animals show some tuning of their sense organs and some specialization of their brains to improve signal detection and characterization.

Detection of sound is often challenging because the received signals are faint and distorted owing to propagation. Sound traveling in air is largely reflected from solid objects, including animals, with little energy transfer. Sound traveling in water is easily transferred to aquatic animals, but because all parts of the animal vibrate in synchrony, there is no immobile reference allowing the animal to detect the vibrations. As a result, animals have had to acquire some very sophisticated adaptations to hear sounds.

Terrestrial animals often have funnel-shaped structures outside the body to collect and concentrate impinging sounds. The funnel shape also creates a gradual change in the properties of the sound-propagating medium from that of air to that of liquid and solid bodies. This increases the amount of trapped sound energy. At the end of the funnel is a thin membrane (called an eardrum) that is set into vibration by the sounds. Small bones or fibres transfer the eardrum movements to a fluid-filled cavity, within which are sensory cells bearing hairlike cilia. As the fluids move, the cilia sway, thereby stimulating the attached nerve fibres. Ears of orthopteran insects (e.g., crickets and grasshoppers) and vertebrates are designed such that different frequencies of sound stimulate different sets of sensory cells. Thus, the animal is able to decompose a complex sound into its component frequencies. This enables the receiver to separate signal frequencies from those of nonsignal sounds. For each band of useful frequencies, amplitudes and a temporal pattern are encoded in the rates and patterns of nerve impulses sent to the brain. Larger animals usually have two ears and use the time delays or differences in signal amplitude at the two ears to identify the direction of the sender. Small animals cannot use this method because the delays and intensity differences are very small. However, they can achieve some directional information by sampling a sound field at several points simultaneously. For example, crickets have their eardrums on their legs, and fine tubes connect each eardrum internally to breathing holes on the sides of their bodies. This allows them to obtain multiple samples of a given sound field at each point in time. Frogs and birds have a space connecting their eardrums that works in a similar manner.

Some aquatic animals have exterior cilia or hairs that sway as sounds pass over them and stimulate sensory cells. This mechanism is effective only within a few wavelengths of the sound source and tends to be limited to lower frequencies. For sound reception at a greater distance from the source, an aquatic animal must create body parts that are moved in different ways during the passage of sound waves. Some bony fish use swim bladders for this purpose. These are air-filled sacs that provide buoyancy. Because air is much more compressible than water, sound trapped by the swim bladder results in much larger molecular displacements than the same sound energy propagating in the rest of the fish’s body. Connecting the swim bladder to the fish’s ears makes it possible for the differences in molecular displacement between the swim bladder and the rest of the fish to be used to stimulate the sensory cells of the ear. This allows a fish far from the sender to detect and measure the passing sound waves.

Animal eyes differ markedly in their range of view, their resolution, and their focusing power. The eyes of vertebrates and cephalopods (octopus and squid) have adjustable lenses that extend the range over which images are in focus. They also have an iris that adjusts the amount of light entering the eye. An effective eye must have many receptor cells if it is to preserve the relative positions of the different objects reflecting light to it. To discriminate between different colours, different receptor cells must be sensitive to different light frequencies. In addition, because light intensities are highly variable, eyes may need different receptor cell types to handle both dim and bright light. Vertebrate eyes use cone receptor cells for bright light and colour discrimination and colour-insensitive rod receptors for dim light conditions. All light receptors contain a protein-bound pigment. This pigment, called rhodopsin, occurs in all multicellular animals. These pigment molecules change shape when absorbing light. This triggers a chain of reactions within the receptor cells ending in the production of nerve impulses. Different photopsins and rhodopsins absorb different light frequencies, permitting receptors to differ in colour sensitivity. Arthropod eyes consist of 8–10 receptor cells clustered around each of many facets, or corneal lenses. It is the number of facets, not the number of receptor cells, that determines visual acuity in arthropod eyes.

Unlike the case with auditory signals, the direction of a visual sender is automatically known once a receiver has detected the signal. The relative positions of receptor cells in an eye are preserved in their projections to the brain. This allows the brain to create a map that replicates, to varying degrees, the visual field of the eye. Projections from the visual maps of the two eyes are compared to identify specific objects and their relative distances. The recognition of patterns is a function of the brain and relies on a combination of inherited and learned mechanisms.

Pheromone reception is accomplished by smell (olfactory) or taste (gustatory) organs. These receptors contain sensory cells with fine cilia, or microvilli, that extend into the medium. Pheromone molecules and other stimuli temporarily bind to specific proteins on the cilia or microvilli. The binding triggers a cascade of chemical reactions within the sensory cell that result in the production of nerve impulses flowing to the brain. The more molecules that bind to a cell, the higher the rate of nerve firing. The sensory cells in an olfactory organ can have highly specific or generalized sensitivities. Specific cells tend to respond only to a certain molecule. Animals often use such cells to detect species-specific mating pheromones. Generalized cells respond to several types of molecules. They are used for less-specific functions, such as the recognition of food items. The olfactory organs of different species vary in the mix of specialized versus generalized sensory cells that they host. Olfactory organs can be as simple as a patch in a mammalian breathing passage or as complex as the plumose antennae of male moths. In some mammals the vomeronasal organ (Jacobson’s organ), located in the roof of the mouth, is used to mediate a behavioral response known as flehmen, in which an animal raises its head and lifts its upper lip in reaction to specific odours. This response requires special movements of the tongue and lips to admit chemical samples to the sensory cells. The vomeronasal organ is the primary receptor organ for many of the pheromones that dictate interactions in mammalian social life, including pheromones involved in conflict, reproduction, and parental care.

Electroreception appears to have been a widespread sensory ability in primitive fishes, in which it was used to detect muscle and nerve impulses in hidden prey. Modern sharks and rays still use this technique for hunting. Mormyriform and gymnotiform electric fish developed these primitive receptors into sophisticated tuberous organs that are used in social communication. These structures, embedded in the fishes’ skin, are encapsulated in ways that make them insensitive to slowly varying electric fields, such as those produced by muscles, but responsive to the rapid discharges of other electric fish. Tuberous receptors are usually tuned to be most responsive to the discharge rate of their own species. The brains of these fish are also highly sensitive to changes in the repetition rates of discharges. This permits sophisticated exchanges between fish during conflicts, courtship, and territorial defense.

Costs and benefits of communication

For both senders and receivers there are costs associated with engaging in communication. It takes time, energy, and special modifications of sender and receiver organs to communicate. Thus, there must be compensatory benefits to each party for communication to be favoured by evolution. A sender will provide information to a receiver only if the decision of the receiver improves the sender’s fitness more than the costs of signaling reduces it. The benefits to the sender may be direct, such as securing a mate or successfully repelling an opponent, or indirect, in that the receiver’s choice may benefit close kin of the sender. A receiver attends to any source of information that is sufficiently reliable, on average, to enhance the receiver’s decision making. The qualifiers “sufficiently reliable” and “on average” reflect the fact that senders may not always send perfect information, but the signals may still be useful to receivers. However, there is a minimum amount of reliable information in any decision situation that must be provided before it is beneficial for either party to engage in communication. Described another way, the payoff to each party (benefits minus costs) must be positive before they will participate in communication.

Animals often have to make decisions in response to alternatives. For example, if a female must determine which of two males will be the better parent for her young, she will mate with the male she deems most fit. In another example, when a parent bird returns to its nest, it must decide which of its nestlings is most needy. It will then give that nestling the worm. The receiver’s decision process begins with some baseline probabilities for each alternative, based on inherited biases, chance, or prior experience. As new information is obtained, whether by examining the candidates directly or by attending to their signals, the receiver updates the probabilities by raising some and lowering others. The receiver’s decision will then be based on these updated probabilities and some knowledge of the relative payoffs of correct versus incorrect decisions.

A number of measures have been proposed for the amount of information provided by animal signals. One measure is relative reliability; this is the increase in the average probability that a receiver makes the correct decision (for itself) when using signals compared to when a receiver is not using signals. Relative reliability also may be weighted according to the relative chances of making the correct decision; this is done by determining the difference in payoffs when making the correct versus incorrect decision. A classical approach computes a logarithmic measure (in bits) of the reduction in a receiver’s uncertainty after receiving and processing a signal. Most of these measures yield similar rankings of the amount of information in signals and differ largely in scale.

Few senders never err in signal selection, and even if they selected the correct signal, transmission can distort signals and cause receivers to interpret them incorrectly. Thus, most animal signaling systems have reliabilities less than that expected for perfect information. Receivers usually have a “best guess” that they adopt when they cannot obtain enough information from a signal to make an informed choice. This best guess is the one that yields the highest average payoff when no signals are available. A receiver that switches from best guesses to a reliance on imperfect signals will start making incorrect decisions, when the best guess was in fact the correct choice. However, the receiver will also start making some correct decisions on those occasions when the best guess was the incorrect choice.

For receivers to participate in communication, the benefits of not making errors when the best guess was wrong must be greater than the costs of occasional errors when the best guess was always correct. As reliability increases, these benefits keep growing and the costs become diminishingly small. Thus, there is a minimal reliability that is required before either party should engage in communication.

Evolution of signals

New signals do not evolve from scratch. As with any adaptation, new signals evolve from existing body structures, organs, physiological processes, and ordinary behaviours that animals already possess for nonsignaling functions. These are sometimes called protosignals. Since the sender can benefit only when the receiver can interpret the protosignal, the receiver must already possess some ability to detect it. Thus, both parties must have prior adaptations that already facilitate the exchange of information. The sender’s protosignal may have been initially poorly associated with the context of interest to the receiver, and the receiver’s reception organ may not have been very effective at detecting the protosignal. However, once such precursors are in place, each party can take advantage of the other, and this can be sufficient to initiate subsequent coevolution of both signal generators and receptors.

Historical scenarios for signal evolution fall into two categories. Scenarios emphasizing sender precursors were a major focus during the early days of ethology in the 1950s and ’60s. The Austrian zoologist Konrad Lorenz, who founded the field of ethology, noticed that the courtship displays of many birds appeared to be elaborated versions of simple preening movements, feeding actions, or nest-building activities. Dutch zoologist Nikolaas Tinbergen, as well as other scientists, provided many subsequent examples of the similarity between mate attraction displays and ordinary survival behaviours. In this scenario, receivers begin to notice actions of other animals because these provide cues about what the other animals will do next. Thus, the protosignals exist prior to receivers’ noticing them. The second perspective, called sensory drive, emphasized receiver precursors for the evolution of signals and was developed during the 1980s and ’90s, spearheaded largely by American biologist John Endler. In sensory drive, signals were viewed as new behaviours or structures that exploit existing sensory biases of receivers. For example, existing female search behaviours for particular foods or offspring might be mimicked by males to get the attention of females for courting. With new DNA (deoxyribonucleic acid) technology for generating accurate evolutionary trees, scientists have been able to trace the histories of signals and receptors using one or both of these scenarios.

Whichever route creates the association between protosignal and context, the subsequent coevolution of signaling and receiving organs tends to follow a similar trajectory. The protosignal often undergoes a reduction in the number of components and an exaggeration of the remaining components in a process called ritualization. Ritualization of visual signals often involves the addition of colour; elongated or erected fur, feathers, and fins; or enlarged body structures that enhance the visibility of the display. As a result of ritualization, auditory signals may be shortened, repeated, or modulated in various ways that make them distinct against a noisy background, and chemical signals are enhanced with structures and behaviours that maximize odour dissemination. The receiver organ may then be fine-tuned to make it especially sensitive to the critical signal components emphasized during ritualization.

Signals that evolve from cues via the sender precursor route are associated with a particular context or meaning from the outset. This evolutionary process is demonstrated by the predator alert signal of Thomson’s gazelles (Gazella thomsoni). A gazelle that has heard a suspicious sound is likely to stop foraging, raise its head high, and stare in the direction of the sound with ears pointed forward. Nearby individuals, spotting the frozen head-high posture, gaze in the same direction and prepare to flee. The freeze reflex has become ritualized and amplified through the evolution of black-and-white stripes along the gazelle’s face and body that make the staring posture more conspicuous.

Intention movements are another widely cited source of signals. They consist of incomplete or preparatory acts that precede major social activities, such as attacking, mating, reconciling, or fleeing. For example, baring teeth, horns, and claws, staring forward, and covering sensitive body parts such as the ears are some well-known precursors for subsequent attack behaviour. Aggressive individuals have ritualized many of these intention movements into signals when both parties benefit by avoiding costly fights. In dogs and cats, the display is ritualized by the exaggeration of lip and nose wrinkling and by the addition of a vocal component. Submissive signals are often the precise opposite in form from a species’ aggressive signals and may consist of an averted gaze or a closed mouth. This contrast between aggressive and submissive signals is called the principle of antithesis and was first noted by British naturalist Charles Darwin in 1872. Other intention movements that have evolved into signals with clear information about what the sender is likely to do next include mating postures during courtship, presentation of nest material to stimulate breeding, outstretched arms to indicate friendly intentions, and head flips by ducks that coordinate taking flight by mimicking the physical act of jumping into the air.

When animals are thwarted in achieving a goal or simultaneously experience two conflicting motivations, such as fear and aggression, they sometimes perform brief, irrelevant behaviours, such as mock feeding, sleeping, or preening. These are called displacement behaviours, and they sometimes become ritualized into displays that appear to indicate the ambivalent state of the sender. In other cases of conflicting motivations, animals may blend two antithetical displays. For example, the broadside threat display often seen in the early stages of a conflict between two competitors in animals such as ungulates, cats, lizards, and fish has been viewed as the blending of aggressive approach and flight. In these animals, the broadside display also presents the largest possible body profile to the opponent, and the display may be thus enhanced with erected fur, feathers, or fins. Aggressive individuals that are fearful of their opponents may also perform displays of redirected aggressive attacks on nearby inanimate objects, reminiscent of an angry person who slams a door instead of causing physical harm to the individual who is serving as the source of frustration. The form of vocal signals can also reveal information about sender state. Vocalizations associated with fear tend to be high-frequency screams because the fearful individual reflexively tenses all of its muscles. This increased muscle tension stretches the membranes used in sound production, causing them to vibrate at higher frequencies. On the other hand, aggressive intent is expressed with low-frequency vocalizations because the threatening individual is more confident and because low frequency is associated with larger body size and thus is inherently more threatening. Some chemical signals are derived from steroid hormones and are used to inform receivers about the sex and reproductive state of the sender. New displays sometimes evolve from other displays in the species’ signal repertoire. For example, a female primate’s copulation solicitation display of rear-end presentation is used in modified form by subordinate males to reduce aggression by dominant males.

Most examples of signal evolution via the receiver precursor scenario involve mate attraction. Tropical anole lizards possess specialized motion detectors in their eyes for distinguishing the jerky motion of their insect prey against the waving motion of the background foliage. The push-up displays of males that are used both to attract females and to repel other males mimic this jerky movement and thus ensure the visibility of their displays. This behaviour is sometimes coordinated with dewlap signaling, in which a male displays a large, colourful throat fan. Many nocturnal moth species have evolved specialized ears for detecting the high-frequency calls of their bat predators. Mate attraction in these moth species is achieved with an olfactory signal, usually given by the female. One group of moths has become diurnal (active during the day) and thus no longer suffers from bat predation. Males in these species have taken advantage of the females’ auditory biases and thus have evolved the ability to produce a high-frequency sound to attract mates. In water mites, tactile animals that do not have eyes or ears, males attract mates by vibrating the water surface with their forelegs—a behaviour that mimics their insect prey. Male mate-attraction signals that evolve via this process are highly species-specific because they are tuned to the receptors of the females of their species.

Signal design rules

The diversity of animal communication signals is enormous. Each signal is assumed to have converged on the form that is best adapted to transmitting the type of information conveyed by that signal in a given social and environmental context. The form of a signal is therefore affected by its modality, the habitat through which it must be transmitted, and the social function it serves. This fact first precipitated a search for general principles of signal design in the 1960s, when American linguist Charles Hockett and American behavioral biologists Stuart Altmann and Peter Marler attempted to come up with lists of design features that could then be used to characterize any type of signal. Once the design feature requirements, or rules, for a given type of signal had been established, the specific mechanisms for satisfying the rules in each modality could be used to determine whether signals serving the same social function in different species exhibited the expected similarities in signal form.

A minimum list of six design features seems to be sufficient to characterize most signals. The range of a signal is the distance that the signal must be transmitted, which is in turn determined by the typical distance between sender and receiver for the social context in which the signal is given. Signal range can be optimized by adjusting amplitude, intensity, hue, size, concentration, and signaling location, depending on the modality. The ability of a signal to be located specifies the degree to which the location of the sender, the receiver, or some external object needs to be encoded in the signal. The form of the signal and the directional capabilities of the receiver’s receptor determine how easily the sender’s position can be estimated, and some modalities have better mechanisms for pointing toward a referent than other modalities. The duty cycle of a signal is the relative amount of time that the signal needs to be on versus off. Some types of signals require on times that are much longer relative to other signals, and the duty cycle can be optimized by adjusting signal duration and repetition rate. The identification level of a signal determines the number of different units that must be distinguished by unique signal variants. Identification levels, listed in order of increasing number of variants required, include species, sex, age groups, colonies, family groups, and individuals. The larger the number of variants the signal must encode, the more complex the signal form must be to generate these variants. In contrast to this between-individual level of variation, the modulation level specifies the degree to which the signal must vary within an individual. Some signals need to encode graded levels of information, whereas other signals need to encode discrete, presence-or-absence information. In addition, the form-content linkage specifies the degree to which the form of the signal is linked to its information content. Signals that indicate what the sender is likely to do next are limited to forms that are functionally linked with the subsequent action, whereas signals that indicate location and identity can have more arbitrary forms.

The design rule for each of these features depends on the signal’s social function. For example, mate-attraction signals are usually given by one sex for the purpose of attracting members of the opposite sex. The information encoded in the signal includes species identity, reproductive maturity, and sender location. Therefore, such signals must be designed to have a large range, good sender-locating ability, high duty cycle, species specificity, and low within-individual modulation. Signals can be arbitrary in form if they transmit only species identity and location. However, if the nonsignaling, choosy sex must select from several signaling suitors, it may seek information about sender quality, health, parental abilities, or other attributes, and the signal will evolve to contain detectable characteristics that are linked to these qualities.

Territory-defense signals inform other nearby individuals that an area is occupied by a defending owner. Territorial signals have many of the same design rules as mate-attraction signals, including long range, high duty cycle, and species specificity. They also can be arbitrary in form, unless they encode information about the vigour or fighting ability of the owner. In order to establish stable boundaries, owners must be able to identify their territorial neighbours, and territory defense signals need to encode individual identity. Territory boundaries may be as important to locate as the territorial owner, a function that long-lasting olfactory marks deposited around the periphery can achieve very efficiently.

Courtship signals are typically given by males once a male and female have approached one another. These signals function to persuade the female to mate, since females are usually more choosy and reluctant than are males. These signals also serve to coordinate the mating act. The range of a courtship signal should be small not only because the sender and receiver are close but also because the mating couple does not want to attract interlopers or predators. Therefore, in most cases, sounds, movements, and scents are low in amplitude. Sender location is generally irrelevant, but in species that lay eggs in specific types of sites, the male may need to point or direct the female to a location he has found or prepared. Duty cycle is typically high for a brief period, and the repetition rate of a signal may increase gradually in order to synchronize copulation, or gamete release in externally fertilizing species. Signals need to be species-specific, and they often need to be sex-specific as well. There may be some need for within-individual modulation if either of the sexes encode their motivation to proceed with the mating. In contrast to fighting or other activities, males often signal their intentions to mate by evolving displays linked to the mating act, and females signal their willingness to mate by assuming a posture that facilitates mating. Courtship generally involves several different signals in multiple modalities, with tactile and olfactory signals often playing an important role. Signal form varies widely, depending on the details of the reproductive biology and habitat of the species.

Threat signals are given when two individuals compete directly and at close range over a nonsharable resource, such as food, a mate, or a territory. With the exception of ritualized fighting, reciprocal communication is used in an attempt to resolve conflicts without fighting; therefore, both individuals are simultaneously senders and receivers. The conflict is likely to be won by the individual that is larger, stronger, healthier, more experienced, or more motivated. Threat signals are designed to transmit information about these sender qualities. Once one contestant decides it would lose during further escalation, it gives a surrender signal to end the conflict. Threat signals share some design features with courtship signals: their range is short; displays are directed at specific individuals; duty cycle is high for a brief period, modulations that encode gradations in motivation are required; and signals are often linked to intentions. However, there are some significant differences. Signals are usually short, forceful, and conspicuous. Identification level involves the recognition of rival status, which may be based on discrete age or sex classes or on a continuous range of classes based on dominance rank or body size. Modulation of threat signals may transmit information about aspects of fighting ability that vary within individuals, such as current condition and motivation. Threat signals are often ritualized intention movements, ambivalent combinations of acts, or redirected behaviours, and some are linked to the size or health of the animal. As with courtship, there are often numerous threat signals in a species’ repertoire, with visual, vocal, and tactile signals providing redundant information about relative motivation and fighting ability.

A final type of signal, one that is observed only in relatively social species, is the alarm signal, which provides information about the presence of a predator or a conspecific rival. There are two different kinds of alarm signals: (1) flee alarms, given in the context of a cluster of animals in immediate danger that cause receivers to rapidly disperse and hide, and (2) assembly alarms, given in the context of dispersed animals that cause receivers to move toward the sender for some type of joint rescue or mobbing response. Design rules are quite different for these two signals. Flee alarms, which are not especially loud because receivers are nearby, are designed to prevent the sender from being located (especially by the predator) and may be linked in form to fearful internal states. Assembly alarms, which have a larger range and longer duty cycle than flee alarms, require that the sender be locatable. The signal is usually repeated and modulated to indicate the degree of urgency. The first real evidence for the validity of design rules was demonstrated with these two types of alarm signals. Many small birds possess vocal alarm signals—one that is directed toward hawks flying overhead and another that is directed toward owls and ground predators, which are often mobbed. Hawk alarms show a striking convergence on a form consisting of a single relatively long high-frequency whistle that has a gradual onset and gradual offset. This is a very difficult sound for a hawk to detect and localize. In contrast, owl alarms consist of short repeated broadband notes that are easy to locate by predator and prey alike.

Honesty and deceit

Senders and receivers may have conflicting interests in the accurate exchange of information. Among humans, it is known that exaggerating and lying can sometimes benefit senders. Animal senders may also gain fitness by cheating under certain circumstances; the strength of the selective pressure to do so depends upon the signaling context and the degree to which the two parties have conflicts of interest. Conflict of interest is greatest when two more or less equal competitors both desire the same nonsharable resource. Each would like the other to back down without a fight, and each would benefit from persuading the other that it is the better fighter by any means possible, including bluffing. In the mate-attraction context, both male and female benefit from mating with the correct species and therefore agree about the accurate transmission of species information. But females may want to mate only with a high-quality male, which puts pressure on low-quality males to hide or exaggerate their quality. An offspring in a multiple brood may exaggerate its need for food to the parent in order to garner a larger share of the food for itself.

The problem of signal honesty is an important issue in studies of animal communication systems. In the early days of ethology, signals were shown to evolve through the ritualization of behaviours that are, or were, functionally appropriate to the contexts in which the signals are given. Signals were believed to be honest indicators of underlying motivations because the signals were derived from physiologically or anatomically linked sources. With the rise of evolutionary game theory in the 1970s, this notion of signal honesty was questioned. British ethologist and author Richard Dawkins and British zoologist John Krebs suggested that senders were best characterized as deceitful manipulators trying to mask their true intentions and trick receivers into actions benefiting senders. Thus, receivers were best viewed as mind readers trying to discount false signals, anticipate the true intent of the sender, and identify their own best countermove. This scenario leads to a never-ending arms race with increasing deceit and concealment of true intentions by senders parried by increased discrimination and exploitation by receivers. Except where sender and receiver have common interests, the resulting signals are largely deceitful and uninformative.

Israeli evolutionary biologist Amotz Zahavi challenged this pessimistic view of signal honesty. He asserted that receivers have the upper hand and should not respond to signals unless they carry some guarantee of honesty. One guarantee is to require that signals impose a cost such that deceitful senders cannot afford to produce an exaggerated signal, or they produce it only in an ineffective way. Signals characterized by such costs are called handicap signals. Although Zahavi’s idea was viewed skeptically at first, subsequent game theory models demonstrated the evolutionary feasibility of handicap signaling, and hence the handicap principle became widely accepted.

A key concept of the handicap principle is that the cost imposed by the signal must be closely related to the sender quality attribute about which the receiver wants information. Although Zahavi proposed that the signal should be designed to “use up” the sender’s quality feature in a display of costly consumption, it is more important that a sender of lower quality with respect to the attribute be less able to afford to produce the signal. Thus, the form of the signal is linked to its information content. One type of cost is energy expenditure. Signals with high production costs can inform receivers about the health, vigour, or foraging abilities of senders. For example, vocal and visual mate-attraction signals must be repeated again and again. Female preference for males that not only produce high-quality displays but also repeat these displays at a high rate will increase the selection pressure on males to perform at the highest possible energetic level they can sustain. Unhealthy or poor-quality males cannot maintain such an expensive display, and this fact will be detectable to females. Choosy females benefit by acquiring vigorous mates that are good genetic fathers and parental providers or possess food-rich territories. Handicap signals also may be given to potential predators. For example, antelopes sometimes perform energetic jumping to approaching predators. Only individuals in good condition can perform these actions well. This provides honest information to the predators that discourages them from chasing the able displayers.

Handicapping is not the only mechanism for generating honest signals. Some signals are constrained by physiology, anatomy, or physical principles to be honest indicators of certain types of sender attributes. Such signals are called unbluffable, or index, signals. Examples of index signals include low-frequency vocal threats that are linked to body size in many vertebrates and tail-beating displays in fish. Likewise, certain forms of ritualized fighting, such as mouth wrestling and antler locking, are index signals of weight and strength. Other signals are associated with aging and health, including song repertoire in birds, which can indicate age, experience, and ability to survive. In addition, pointing displays that indicate the direction of gaze and olfactory signals that are related to reproductive physiology are considered index signals.

True threat signals of intention to attack require very effective honesty guarantees if they are to convince rivals to retreat. Otherwise, an initially honest signal will be invaded by bluffers that give the signal but never follow through with an attack. In this case the sender must demonstrate its sincerity by approaching the rival very closely. Only a threat display performed within close proximity to the rival, where there is the risk of a retaliatory attack, will be taken seriously by the receiver. Threat displays are typically attack-preparatory postures performed close to the rival, giving the sender both a tactical advantage and demonstrating its willingness to take risks.

Some communication signals are not costly to produce, risky to execute, or obligatorily linked with physical properties of senders. The code by which these signals are associated with contexts is an arbitrary convention, and these are therefore called conventional signals. If there is no conflict of interest between sender and receiver, senders will not be tempted to cheat; conventional signals can be honest and stable without further guarantees. However, conventional signals also are seen during conflicts of interest, and in this case there must be a stabilizing cost that maintains honesty. Conspicuous colour patches in some birds and lizards are the classic example of this type of signal. The size or hue of the patch is correlated with the dominance rank of the individual, hence the designation of these patches as badges of status. Large badge size deters aggressive challenges by small-badged individuals. The cost of guaranteeing honesty of a large badge is aggressive retaliation from other large-badged individuals. The evolution of such signals must be accompanied by frequent testing of the honesty of other individuals with a badge size similar to one’s own while avoiding or ignoring individuals with larger or smaller badges. Such a rule makes it very dangerous and costly for a low-status individual to cheat by sporting a large badge.

Most signals are believed to be honest most of the time because conflicts of interest are minimal or because appropriate costs are imposed on cheaters. The best demonstrations of honest signaling have been described for handicap signals of mate quality. One well-documented example is the elongated tail feathers of the barn swallow (Hirundo rustica), studied by Danish zoologist Anders Møller. Females prefer males with longer tails, pairing very quickly with males having artificially enlarged tails compared with males with shortened tails. Long tails are a handicap for males. Barn swallows are aerial foragers that capture flying insects on the wing, and artificial tail elongation increases the drag on the tail and reduces agility and foraging efficiency. Males with naturally long tails are stronger, healthier, and resistant to parasites. These individuals not only grow long tails and cope with the foraging handicap but also transmit parasite resistance to their genetic offspring. Females obtain better-quality offspring by selecting long-tailed males. Other examples of honest mate-quality signals preferred by females include red plumage coloration in the male house finch (Carpodacus mexicanus), which is correlated with a male’s foraging skill and survivorship; long call duration in the gray tree frog (Hyla versicolor), which is energetically costly for males but associated with better survivorship in their offspring; and high display rate in damselfish (Stegastes partitus), which is correlated with the survivorship of the eggs that the male tends.

Dishonest signaling does occur. Deceit is the provision of inaccurate information by the sender such that the sender benefits from the interaction but the receiver pays the cost of a wrong decision. Types of deceit include lies (using the wrong signal among an unordered set of alternatives), exaggeration or bluff (using a signal whose rank among ordered alternatives is different from that for the corresponding condition values), and withholding information (not giving a signal when appropriate). There are numerous examples of predatory species that mimic the mate-attraction signal of their prey, but in interactions between two different species; there is no selection pressure on the predator to be honest, and there is little the prey can do to avoid being exploited. The prey, as receiver, can try to improve its discrimination between true mates and impostors, but this process will simultaneously select for better mimicry by the predator.

Within-species deceit is a different matter, since dishonest signaling can sometimes backfire on the sender. For example, an outright lie has been described in birds foraging in flocks, where one individual may give a false alarm call to scare competitors away from a rich food find. A sender cannot “cry wolf” too often, however, because receivers may learn to ignore the signal, and the signal will thus cease to be effective in true alarm contexts. Bluffing threats sometimes occur in mantis shrimp (Gonodactylus bredini), which defend their burrows from intruders with a claw-spreading display. Recently moulted individuals that are soft and unable to defend themselves effectively may nevertheless sometimes give the threat display in the hope that an intruder will not press an attack. Withholding information has been described in primates that fail to advertise a rich food find. If other group members catch an individual feeding on such a find, the individual is aggressively punished. Thus, low levels of dishonesty may persist in many signaling systems. However, signals must be sufficiently reliable and honest most of the time; otherwise, they will be discounted and ignored by receivers, senders will no longer benefit from giving dishonest signals, and the signals will disappear from the species’ repertoire.

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