Introduction to Ethology

Ethology is the zoological study of animal behavior. Ethologists have a special interest in genetically-programmed behaviors known as instincts. The predictable behavioral programs are inherited by animals through their parents and portions of the programs are open to natural selection and modification. Thus, these behaviors are phylogenetic adaptations that have an evolutionary history. This often leads to a comparative approach and has led researchers to search for the biological basis of human behavior by comparing our activities to those of our close relative (other primates; especially chimps).

There are two schools of thought as to how animals acquire their behavior patterns. Some hold to the view that animals, including humans, learn all their behavior during the course of ontogenetic development. Ducks, for example, learn how to quack like a duck and don't honk like a goose because they hear their parents while within the egg). Experiments have since shown that these behaviors are built-in and not learned.

Very complex behavior patterns can be passed on through the genes. A spider's orb web, for example, is built perfectly the first time a spider attempts construction, despite the fact that they may have no prior experience with webs (Fig 1). Female spiders construct egg sacs in the Fall, and then die. The spiderlings emerge in the spring, and never had experience with an orb web before building their own.

Ethology differs from the study of Animal Behavior, in that animals behaviorists generally are interested in learned behaviors while ethologists concentrate on innate behaviors. Also, animals behaviorists tend to be trained in psychology, while ethologists are zoologists. Animal behaviorists tend to work with "bright" animals, such as rats; putting them through trials with mazes and Skinner boxes. While the study of learned behavior is both important and immediately applicable to human psychology, these behaviors cannot have an evolutionary basis (other than the neural capacity to learn)

Konrad Lorenz, along with Karl von Frisch and Nikolaas Tinbergen are generally recognized as the "fathers of ethology" (read Lorenz's 1973 Nobel Prize acceptance speech here which he shared with Karl von Frisch and Nikolaas Tinbergen; Fig 2). But the origins of ethology can be traced back to Charles Darwin and his work on the expressive movements of man and animals (the full text is available here). Darwin was the first to use a comparative phylogenetic method in the study of behavior.

No discussion of ethology would be complete without mentioning Irenäus Eibl-Eibesfeldt, who was the first to successfully apply ethological methods to the study of human behavior (Fig 3). He carefully recorded the activities of humans using a side-viewing camera so the subjects didn't know they were being observed (Fig 3). By comparing gestures and body language across cultures, he identified numerous innate behavior patterns in humans.

Much of the work in ethology revolves around problems in animal communication. In fact, this is the work for which von Frisch is best known. He teased apart the "dance language" of bees (Fig 4). Worker bees dance to communicate the distance, direction, and quality of a feeding place they have found while foraging around the hive. The dance is performed on the vertical comb of the hive. If the feeding place is directly toward the sun, the bees dance up (fig 4a). If the feeding place is directly away from the sun, they will dance down (fig 4d). Angles to the sun are communicated as shown in figure 4 (b & c). As the sun moves across the sky, the bees adjust their dance so that the direction is always up-to-date. If, for example, a bee finds food at sunrise and indicates that it is located directly toward the sun (by dancing up; fig 4a), by the time the sun sets, the bee will be dancing down. Thus, bees have an internal biological clock that tells them where the sun should be in the sky without them having to go out and check.

Distance to the feeding place is communicated by the number of waggles at the center part of the dance. More waggles indicate greater distance. Sites with lots of high quality food are communicated by the vigor of the dance (very good sites produce frantic dancing). In addition, other workers paying attention to the dancer touch their sister and can determine what type of flower she visited by the pollen stuck on her hairs. A second dance, a round dance, is used when the food source is very close to the hive.

The type of communication an animal uses can be described by the sensory modality used to receive the signal. Examples can be seen in the following table:

Sensory Modality	Example
Chemoreception	Pheromones (group cohesion, territory marking, individual recognition, sex pheromones, etc.)
Mechanoreception	Vibrational cues including substrate-coupled (spider on web) and sound (bird and cricket song)
Visual	Bird courtship dances, aggressive stances of canids, firefly light patterns.
Electrical	Electric eels and weakly electric fish communicate with one another through charged pulses.
Psychic	That's how those voices in your head get there!

CHEMICAL COMMUNICATION
Pheromones are chemical "perfumes" that one animal emits to influence the behavior of another. The pheromones can be classified according to the mode of reception (contact vs. airborne) or by their function (sex pheromones, aggregation, territorial, recognition, etc.). Figure 5 shows an adult male Rabidosa rabida wolf spider following the dragline of a conspecific (same species) female. Both males and females lay out dragline as they move about. During their mating season (late summer or early fall, depending on the latitude), males find females by stumbling across their dragline. Pheromones deposited on the line alert the male that it was deposited by an adult female of his species and he'll follow it using his palps (the little leg-like structures at the front of the spider.

A close-up scanning electron micrograph of a male's palp can be seen in Figure 6 (click to enlarge). This is a left palp. At least two types of hairs are apparent on the palp. The more numerous pointed hairs are mechanoreceptors (a sense of touch for the spider). The brighter, less numerous, and curled hairs are chemoreceptors. Notice that the chemoreceptors. are found on the medial side of the palp (toward the upper left); that part of the palp used for following female's draglines. A closer view of the hairs are shown in the second image of Figure 6. In the second image, the curled hairs are the chemoreceptors, the straight ones are mechanoreceptors. Note that both are inserted in sockets in the animal's integument to allow them to swivel when touched.

Click here for an animation showing a male silkworm moth (Bombyx mori) following a female moth's odor trail.

Chemical communication has been found in nearly all organisms investigated, including fungi, bacteria, protists, and plants. Among the animals, nearly all use pheromones to one level or another, with the notable exception of most birds. While animals such as spiders and insects tend to use pheromones with simple chemical structures, mammals use pheromones composed of a complex "cocktail" (with the exception of the social insects (Fig 7). Additional information on pheromones in mammals, with special reference to humans can be found here.

MECHANICAL COMMUNICATION
Communication through vibrations may be either substratum-coupled (through vibrations in the ground or other substrate), or acoustic (through the air or water). Among spiders, web vibrations are used to communicate between a courting male and the web's owner (he plucks out a song) or to determine the type and placement of prey that have blundered into the web. To measure web vibrations in the lab, we use a laser system coupled to a computer (Fig 8). Vibrations of the web are picked up by a phototransistor whose output is sent to a computer through a digital-to-analog converter (DAC). As the web vibrates, different light intensities are reflected on the solar cell, producing a change in the voltage. This voltage change is assembled by the computer into a vibrational waveform.

The web vibration patterns differ among species (Figure 9). The image on the left is for Pholcus opilionoides while that on the right is for Achaearanea tepidariorum. Click to hear the web vibrations of Achaearanea tepidariorum. Other animals that use a substratum-coupled vibration system for communication include water striders and leaf hoppers.

Acoustic communication is accomplished as vibrations through air. Spiders also use sounds for communication (listen to a male's courtship song here:

). An oscillogram (top) and spectrogram of the courtship song you just heard is shown in figure 10. The oscillogram shows the pattern of pulses used by Rabidosa rabida males to communicate with females. The lower spectrogram shows the timing of the pulse (along the X axis), the frequency (along the Y axis; lower frequencies at the bottom), and intensity (by the darkness of the traits; red is loudest). You can play with a reverse spectrograph here.

Compare the relatively simple sonogram from the spider to that of a redwing blackbird:

(Fig 11). An oscillogram and spectrogram of the song are shown in Figure 12. Note the richness of the spectrogram compared to that of the spiders. An example of a male and female redwing "discussing" their relationship can be found here:

. More insect sounds can be found here. More bird song recordings are here and here.

VISUAL COMMUNICATION
With good vision, it became possible for many animals to use a new channel for communication. Among those spiders that have good vision, courtship dances perfumed by male spiders help to get the female in the mood. Figure 13 shows a movie of a male spider performing part of his courtship dance. The is from a female's view. Doesn't do much for me, but it sure gets her attention.

Other animals have more spectacular, albeit still silly, courtship dances (Figure 14).

Competition among males for the most impressive displays to attract females has led to ornaments, colors, badges, and other decorations to attract females and/or ward off other male competitors. The red epaulets of the redwing blackbird, for example, are necessary for male birds to defend their territory. If the epaulets are painted black, the male can no longer chase off competing males (in fact, he is not taken at all seriously and is completely ignored by his rivals). Among other animals, the need to impress females has gone to an extreme (Figure 15). The male peacock, for example, is required to put up with his ungainly and brightly-colored tail and accessory plumage to impress females. This is despite the fact that these feathers make him more susceptible to predation and are metabolically expensive to construct.

The Irish elk (Fig 15) is now extinct, and has been since the end of last ice age. During the ice age, competition among males and selection by females resulted in huge antlers used for display and defense. When the glaciers retreated, forests grew in their place, and the huge antlers became a liability since the males couldn't move among the densely-packed trees without catching their heads. This ultimately lead to the extinction of the species.

Generally, sexual selection leads males to extremes and is driven entirely by female preferences and competition among males for mates (Fig. 16). This has produced some extremely silly looking and conspicuous males over evolutionary history (Figure 17).

IMPRINTING
A specialized type of "programmed learning" seen in many higher animals is a process known as "imprinting". The first experimental analysis of imprinting was done by Konrad Lorenz on geese hatchings( Figure 18). The first job of a gosling is to identify it's mom so they can follow her should she start to wander off. Goslings are pre-programmed to follow the first object producing the species specific call. This object is then identified as "mom". It doesn't matter what the object is, just as long as it emits the proper call and moves. Researchers have had fun with this effect by imprinting ducklings on a model train that emitted quacks from the speaker. Ducklings would dutifully follow the train just as if it were mom.

Another characteristic of imprinting is that this specialized learning must occur within a certain time-window known as the "critical period". Ducklings that are first exposed to mom at 1 week of age will not follow here, since that is outside the critical period for learning the task.

Song learning in some birds (doves, for example), is entirely innate. Young doves raised without exposure to adult song will sing the adult song perfectly the first time they try it. Most other birds, on the other hand, need exposure to the adult song during a narrowly-defined critical period in order to imprint and learn the proper song.

Swamp sparrows and song sparrows have a species-specific song (Figure 19). The swamp sparrow song consists of a trill of nearly identical syllables delivered at a constant rate. Song sparrows produce a more complex song consisting of a trill followed by a melodious note phrase. Young swamp sparrows raised in the absence of adults sing a still produce a trill, but of less complex syllables (the innate song). Similarly, song sparrows produce an innate song that has some of the characteristics of the normal song.

Researchers have raised birds with and without the experience of hearing their species-specific song (Figure 20). Regardless of the chicks' experience, young birds all sing a variety of "call notes". In figure 20, each of the symbols represents a different musical motif. Note that the experience of the animal doesn't affect this aspect of song development. If, however, a hatchling hears the adult song within the critical period (10 - 30 days in this example), they go through babbling and subsong stages differently so that, by the time they reach adulthood, their full song is very similar to the song they heard during the critical period. In this example, there are slight changes in the song motifs

and

. These song structures are similar to the original and differ only in timing, the range of notes used, or some other minor feature.

These slight differences in song structure impart individuality to the songs, or dialects (Figure 21, 23). The slight differences allow neighboring birds to recognize one another as individuals. Birds stake out their territories by singing. After the territories are agreed upon, it is to everybody's advantage to recognize neighbors. This way, a bird that hears a neighbor's call knows that he doesn't have to pay special attention to the situation since the territorial boundaries have already been agreed upon. Only when a stranger enters the territory and begins to sing does the male have to give it special attention (by chasing the interloper off).

Note that some of the song motifs have a genetic component. The motif

, for example, shows up in birds under both experimental conditions. Those with no song experience, however, sing a slightly different musical phrase (

) vs. the

structure for those with song experience). If the chicks hear the song outside the critical period (before day 10 or after the first month), the lesson doesn't stick. These birds will sing as if they never heard the adult song. Figure 23 shows the sonograms for birds with different experiences during the critical period.

How does a young bird know which noises to pay attention to? Why doesn't a young Robin, for example, pick up the species song of a Blue Jay, or for that matter, a car horn? The answer is that the young bird has some idea of what to listen for - an innate "neural template" that gives the general parameters of the species-specific song (Figure 24). The neural template theory suggests that the songs of unrelated birds (

) do not fit the general configuration of genetically predisposed song structures (

). The template (or idea of how the species song should sound) is slightly sloppy; allowing for the creation of dialects and individual, bird-specific songs.

Another example of restricted learning is food aversion. Animals that eat a novel food and then get sick will avoid that food from then on. In this example, a Blue Jay has eaten a Monarch butterfly. Monarch butterflies feed on milkweed as larvae and concentrate milkweed chemicals in their skin. These chemicals make anyone who eats a monarch sick (at the very least; the toxins are cardiocides that attack the heart). Birds that have experienced the stomach upset brought on by eating Monarchs will avoid Monarchs from that day on.

OTHER AREAS OF RESEARCH IN ETHOLOGY
Comparative ethology: The head-up posture is a widespread signal in fighting behavior in many passerine families (Fig 18). The evolutionary explanation for this common behavior is that they all share a common ancestor that performed this behavior. The right image in figure 26 shows nine oscillograms for species of cicadas found in Ceylon. The time markers are 0.5 sec.

Perceptual Systems of Animals. The flowers in figure 27 were drawn from photographs with a quartz lens to pass visible and ultraviolet light. The first picture is with a yellow filter , the second with an ultraviolet filter. In Helionthus (above) and Octenthera (below), striking ultraviolet patterns emerge that are invisible to humans. These patterns are easily visible to a bee's eye.

Analysis of Behavior Patterns: The sequence of activities during courtship of stickleback fish includes much aggression (Fig 28). The sequence of male courtship activities from dancing to fertilization are shown. The number of times that these behavior patterns preceded or followed other actions is represented by the width of the connecting arrows. Attacks may follow any part of the sequence.

Play Behavior: Many animals play, not only as young, but also as adults. Play behavior is thought to solidify social bonds, clarify rank within a social group, and prepares young for sexual and predatory behaviors. A common signal used to elicit play among animals is the butt-up display (Fig 29).

A rather amazing example of the power of this signal is shown in figure 30: The end seemed VERY near for Hudson, a Canadian Eskimo dog tethered near the shore of Hudson Bay east of Churchill, Manitoba. A thousand-pound polar bear was lumbering toward the dog and about 40 others, the prized possessions of Brian Ladoon, a hunter and trapper. It was mid-November 1992; ice had not yet formed on the bay, and the open water prevented bears from hunting their favorite prey, seals. So this bear had been virtually fasting for four months, Surely a dog was destined to become a meal.The bear closed in. Did Hudson howl in terror and try to flee? On the contrary. He wagged his tail, grinned, and actually bowed to the bear, as if in invitation. The bear responded with enthusiastic body language and non-aggressive facial signals. These two normally antagonistic species were speaking the same language: "Let's play!" The romp was on. For several minutes dog and bear wrestled and cavorted. Once the bear completely wrapped himself around the dog like a friendly while cloud (top), Bear and dog then embraced, as if in sheer abandon (bottom), Overheated by his smaller playmate's shenanigans, the bear lay down and called for a time-out.

Ethology has moved into a technological direction. Ethologists are picking apart the neuro-endocrine basis of behavior (Fig 31) to explain the proximate reasons behind why animals act they way they do. There is also a movement to mechanize data collection so human error can be removed and strict statistical tests can be performed on raw data (here and here) Researchers have also begun to use molecular biology techniques to extract genes that control particular behaviors (an example is here).

THE STUDY OF HUMAN ETHOLOGY
Listen to "Human Behavior" (from the Human Ethology Film Archives). One of the methods used in human ethology is to compare the behavior of our closest relatives to our own to understand the origins of human behavior (much as one would for the birds in Fig 26). As mentioned previously, Charles Darwin was one of the first to recognize the value of the comparative approach. Figure 32 shows a sketch from the text The Expression of Emotions in Man and Animals. From this drawing, it is clear that a common ancestor of chimps and humans shared these expressions. Similarly, the origins of nonverbal communication, contact behavior, and social grooming are explored using the comparative approach (Fig 33). Another method is to compare the behavior of normal children to that of children with congenital sensory deficits (Fig 34 -36).

In the above three figures, it is thought that these behaviors could not have been learned because of their complexity and since the children are deaf and/or blind. The behavior of the infant in figure 27 is especially striking. Note the open-mouthed play face, smiling, and eye fixation toward the mother. The complexity of these expressions, along with the eye fixation suggests that these behaviors are instinctive. In figures 28 and 29, deaf-blind children show facial expressions they have never had an opportunity to see. In addition, their vocalizations are appropriate to their emotional state. Watch Smiling by a Deaf-Mute Boy (from the Human Ethology Film Archives).

The third method used by human ethologists is to compare behaviors across cultures. If the behavior shows up in many cultures, then it is more likely to be a biological trait, rather than a learned cultural trait. One of the first behaviors documented to occur across cultures is the "eyebrow flash"; used when one greets a friend (Fig 37). Watch an Eyebrow Flash (from the Human Ethology Film Archives). See also a Himba flash.

Coy or flirtatious behavior is also seen across cultures. Typically, the female looks sideways at the male until she catches his attention, Then she turns away and down with a smile, usually while maintaining eye contact. She then turns again toward the male, shows a full smile, but either covers it with her hand or by looking down. These behavior patterns are only seen in females and show up very early in their development. Examples of coy or flitertous behavior is shown in figure 38. You can watch an example of coy behavior here (from the Human Ethology Film Archives).

Another example of flirtatious behavior can be seen in figure 39. The male and female were told to wait in the room before being given a completely unrelated test. They were unaware that their behavior was being filmed. The female is mid-way through a "head toss"; a behavior that flings her hair toward the male and has been interpreted as flirtatious. The second image is a difference image. The difference image is constructed by subtracting the prior frame of the video from the current frame. Objects that do not move are subtracted from one another and disappear. Moving objects show up as dark areas, with the greatest darkness correlated with the greatest movement. Acceleration of the female's hair calls attention to it. You can watch this interaction between a male and female, see the difference movie or get the more information.

Figure 40 shows some frames from a female turning in front of a male. The set-up for this film was to tell the female subject simply that the study was involved in movement. The female then turned. Afterward, the researchers determined where she was in her cycle. Data indicate that small movements and their quality are linked to physiological states. Under high estrogen levels, movements are slower and show a higher information content per time (essentially, "look at me!"). In 33A, her hair, breasts, and body line are accented. In B, the hair and body line are accented. In C and D she's showing off her rear end and small of her back. This is all unconscious display on her part. You can see the original movie here, the difference move here (both require QuickTime. Get that here).