Communication and Animal Signals

If the hyena’s genital display is really a form of communica- tion, then the sender (the hyena with an erection) is using its genitalia as a signal (a specially evolved message that contains information) to modify the behavior of the receiver (the inspector hyena). Central to this definition of communication is the “spe- cially evolved signal,” which eliminates cases where the behav- ior of one animal influences that of another without an evolved message being involved. For example, a mouse making rustling sounds while foraging at night is not communicating with an owl that is hunting it by listening for the mouse’s sounds. To under- stand which types of interactions constitute communication and which don’t, and to determine how communication systems evolve, we must recognize that the transfer of information from a sender to a receiver—whether intentional or not—can positively or negatively affect the fitness of both individuals.

FIGURE 8.2 outlines a framework for understanding communication from this cost–benefit perspective. When both the sender and the receiver obtain a fitness benefit (+/+), we refer to this interaction as honest signaling (which is sometimes referred to as true communication; Bradbury and Vehrencamp 2011). Honest signaling evolves as a cooperative interaction between two individuals. When a sender uses a specially evolved signal to manipulate the behavior of a receiver such that the sender receives a fitness benefit but the receiver pays a fitness cost (+/–), we call this deceitful sig- naling (or manipulation). Both honest and deceitful signaling are forms of commu- nication because in both cases the sender uses a specially evolved signal to positively influence its own fitness. When the sender pays a fitness cost but the receiver receives a fitness benefit (–/+), we refer to this as eavesdropping. In the example of the mouse and the owl, the owl was eavesdropping on the mouse, whose rustling sounds were an incidental transfer of information to the owl called a cue, an unintentional transfer of information (which is different from the intentional transfer of information in a signal). Unlike honest and deceitful signaling, eavesdropping involves information transfer via cues rather than signals. Communication systems in which both individuals pay a fitness cost (–/–) are unlikely to evolve. And you should know why.

Information Use and Animal Signals

Information is critical to survival and reproduction because it helps individuals adjust to changing social and ecological circumstances (Dall et al. 2005). For example, individuals need to decide where to settle, where to forage, and with whom to breed, and having more information allows them to make more knowledgeable decisions. Animals communicate information about the world around them (such as where to find food), as well as information about themselves that can be stable over time or that varies over longer or shorter time periods (Bradbury and Vehrencamp 2011). Stable information includes things such as species identity, sex, and toxicity, whereas states such as physiological condition (e.g., hunger, health status) and dominance rank can change from season to season or even minute to minute. As you learned above, information transfer is critical to communication because it can directly influence the fitness of both the sender and the receiver. Senders may be attempting to transfer either motivational information about themselves (for example, when courting a potential mate) or referential information about a specific object (for example, when warning others about a predator; Donaldson et al. 2007). Despite some criticism that it is too restrictive and should instead acknowledge the different roles and often divergent interests of signalers and senders that can yield fundamental asymmetries in signaling interactions (Rendall et al. 2009), an information-based framework of communication integrates signal reliability with receiver decoding, decision making, and fitness consequences into one measure that is subject to selection (Bradbury and Vehrencamp 2011).

FIGURE 8.3 The round dance of honey bees. The dancer (the uppermost bee) is followed by three other workers, which may acquire information that a profitable food source is located within 50 meters of the hive. (From von Frisch 1965.)

The communication framework detailed above gives behavioral biologists the ability to identify the information being transmitted and how it affects both the sender’s and the receiver’s fitness. Take for example, the elaborate dances of the honey bee Apis mellifera. Dissecting this form of referential signal allows us to explore not only who is communicating, but what they are communicating about (the message) and how this influences the bees’ fitness. These dances are performed by foragers (senders) when they return to their hive after finding good sources of pollen or nectar and are directed toward other workers (receivers) (von Frisch 1967). As the dancers move about on the vertical surface of the honeycomb in the complete darkness of the hive, they attract other bees, which follow them around as they move through their particular routines. Researchers watching dancing bees in special observation hives have learned that their dances contain a surprising amount of information about the location of a new food source, such as a patch of flowers. If the forager executes a round dance (FIGURE 8.3), she has found food fairly close to the hive—say, within 50 meters of it. If, however, the forager extends the round dance into a waggle dance (FIGURE 8.4), she has found a nectar or pol- len source more than 50 meters away. The longer the waggle-run portion lasts, the more distant the food. Thus, the target distance—up to 10,000 meters—is encoded in the duration of the waggle run.

Knowing how far the food is from the hive only matters if the bees know which direction to fly. Luckily, this too is encoded in the waggle dance. By measuring the angle of the waggle run with respect to the vertical, an observer bee (or human) can tell the direction to the food source. A foraging bee on its way home from adistant but rewarding flower patch notes the angle between the flowers, hive, and sun. The bee transposes this angle onto the vertical surface of the comb when she performs the waggle-run portion of the waggle dance. If the bee walks directly up the comb while waggling, the flowers will be found by flying directly toward the sun. If the bee waggles straight down the comb, the flower patch is located directly away from the sun. A patch of flowers positioned 20 degrees to the right of a line between the hive and the sun is advertised with waggle runs pointing 20 degrees to the right of the vertical on the comb. In other words, when outside the hive, the bees’ directional reference is the sun, whereas inside the hive, their reference is gravity.

The conclusion that the dances of honey bees contain information about the distance and direction to good foraging sites was reached by Karl von Frisch after years of experimental work (von Frisch 1967). His basic research protocol involved training bees (which he marked with dots of paint for individual identification) to visit feeding stations that he stocked with concentrated sugar solutions. By watch- ing the dances of these trained bees, von Frisch saw that their behavior changed in highly predictable ways depending on the distance and direction to a feeder. More important, his dancing bees were able to direct other bees to a feeder they had found (FIGURE 8.5), leading von Frisch to believe that bees use the information in the dances of their hive mates to find good foraging sites. Many years later, Jacobus Biesmeijer and Thomas Seeley were able to show that more than half the young worker bees that were just beginning their careers as pollen or nectar gatherers spent some time following dancing bees before launching their collecting flights (Biesmeijer and Seeley 2005). This finding suggests that dance information really is useful to bees about to start foraging for food.

In addition to obtaining distance and directional information from the waggle dance, bees may obtain otehr info from the waggle dance. There is some evidence that recruits learn the odors of collected food from the dancers they follow. Receivers make contact with the dancer’s body parts where food odors are most intense, such as the mouthparts and hindlegs. Some bees appear to rely more on the signals in the dance, while others rely more on the food odors. The waggle dance also helps modulate the readiness of bees to respond to the spatial information encoded in the dance (Gruter and Farina 2009).

The dances of the honey bee illustrate how animals communicate referential information about their environment. This includes not only searching for food in the case of the bees, but things such as producing alarm calls to warn others about approaching predators. One of the best studied of these referential alarm calls is that of the vervet monkey (Chlorocebus pygerythrus). Robert Seyfarth, Dorothy Cheney, and Peter Marler demonstrated that vervet monkeys living in the Kenyan savanna have distinctive alarm calls that signal different types of predators and classes of external danger (Seyfarth et al. 1980). By recording alarm calls made in the presence of leopards, eagles, and snakes, and then playing those calls back in the absence of predators, the researchers demonstrated that monkeys responded very differently to the different types of alarms: when played a leopard alarm call, monkeys ran into trees; when played an eagle alarm call, monkeys looked up or ran for cover; and when played a snake alarm call, monkeys looked down or approached the source of the signal, presumably to mob a snake if they encountered one. Thus, each call conveyed different information about the type of predator, and receivers interpreted these varied signals and responded differently to each one.

FIGURE 8.4 The waggle dance of honey bees. As a forager performs the waggle-run portion of the dance, she shakes her abdomen from side to side. The duration and orientation
of the waggle runs contain information about the distance and direction to a food source. In this illustration, workers attending to the dancer learn that food may be found by flying 20 degrees to the right of the sun when they leave the hive. (A) The directional component of the dance is most obvious when the dance is performed outside the hive on a horizontal surface in the sunlight, in which case the bee uses the sun’s position in the sky to orient her waggle runs directly toward the food source. (B) On the comb, inside the dark hive, dances occur on vertical surfaces, so they are oriented with respect to gravity; the deviation of the waggle run from the upward vertical equals the deviation of the direction to the food source from a line between the hive and the sun.

FIGURE 8.5 Testing directional and distance communication by honey bees. (A) A “fan” test to determine whether foragers can convey information about the direction to a food source they have found. After training scout bees to come to a feeding station at F, von Frisch collected all newcomers that arrived at seven feeding stations with equally attractive sugar wa- ter. Most new bees arrived at the feeder in line with F. (B) A test for distance communication. After training scouts to come to a feeding station 750 meters from the hive, von Frisch collected all newcomers arriving at feeders placed at various distances from the hive. In this experiment, 17 and 30 newcomers were captured at the two feeders closest to 750 meters, far more than were caught at any other feeder. (After von Frisch 1965.)