Imagine that you are sitting at your kitchen table. It is a beautiful summer morning; the door slaps shut after the dog has pushed it open with her nose to go outside. As you take your first sip of coffee, a housefly that entered when the dog exited suddenly claims your attention. Like a tiny vulture, the fly circles above the table, slowly descending, until she lands close to the sugar bowl. The fly walks toward the bowl, and stops by a few grains of sugar that you spilled when you lifted your spoon from the bowl two minutes earlier. The fly inflates her proboscis and begins to dab at the sugar. As you watch this, you begin to feel a mild sense of outrage, not because the fly is stealing sugar, but because the fly’s moist, spongy proboscis, now dabbing at your table, was recently outside, probably dabbing at dog feces or the rotting chicken in the rubbish. You wave your free hand at the fly; she jumps into the air and hovers nearby before quickly landing back at the sugar. You bring your hand rapidly down, attempting to crush the fly, but she is too quick for you. You put your coffee cup down, rise, and reach for the flyswatter, a tool that humans, with their big brains, have invented to crush flies. The flyswatter doubles the effective length of your forearm and so doubles the speed of your strike. The fly has resumed dabbing at the sugar. You strike. The fly sees the rapidly approaching head of the flyswatter. She jumps and begins to fly, but the broad head of your simple tool stops her flight and smacks her with enormous force into the table. Her internal organs, including her brain, are crushed beyond repair. A tiny marvel of miniaturized circuitry and engineering lies mangled on your table. In your own brain, the circuits that would trigger shame or remorse do not light up. You brush the carcass to the floor and step toward the door, where the dog is scratching to be let in.
The first thing to say about this ordinary moment in life is to note the extraordinary performances of you, the fly, and the dog. The three of you used sensors that are tuned to radiation in certain parts of the electromagnetic spectrum, as well as sensors (in the dog and the fly) tuned to detect certain chemicals in the environment, to extract useful information about your environments. Your brains then issued precise sets of commands to muscles that pulled in a complex way on your skeletons, causing your bodies or parts of your bodies to move through space in a smooth, goal directed way.
W.T. Thach, a neurobiologist who studies the cerebellum, a part of the brain that controls movements, once remarked that, “Moving the skeleton is an engineer’s nightmare.” Yet animals, such as you, the dog, and the fly, make smooth, precisely timed and impeccably directed movements. The way that each of you produces movements is essentially identical. You, the dog, and the fly have sense organs that transduce environmental energy or materials into patterns of nerve signals. Each of you uses sense organs, called eyes, to transduce light energy from a narrow band of the electromagnetic spectrum. Each of you has sensors that bind to certain chemicals in the environment and transduce this event into patterns of nerve signals. For you and the dog, these chemical sensors are in the nose; in the fly, the sensors are on many parts of the outer body, including the feet – that’s how the fly knew to stop and extend her proboscis when she walked into that sweet spot on your table.
Each animal species also has a rich variety of internal sensors. You and the dog have receptors that report on blood temperature, sugar level, and acidity, the amount that each muscle is stretched, the likelihood that damage is occurring, mechanical pressure at most parts of the skin, how much the muscular walls of each blood vessel are contracted, and the position of your head and eyes, to list a few examples. The internal sensors report on the biochemical and mechanical integrity of the body, as well as on body part position. All these reports, from the sense organs and from the internal sensors go, in you, the dog, and the fly, to the brain.
A brain is an integration and command center. It receives reports from the sense organs and the internal sensors, integrates the information to create priorities and then, based on the priority list, issues commands. These commands are of two sorts. First, there are commands to the organs – to the heart, lungs, gut, blood vessels, and endocrine glands. These commands are concerned with the essential task of keeping the body running. However, as we saw in our summer tableau, an animal must do more than simply rest, plant-like, in a steady state; it must also move through its environment. This is where the second sort of command comes in. These are the commands to the muscles that pull on the skeleton and produce movements. These movements are known as behavior.
Muscle tissue is evolutionarily ancient and operates the same way in all animals. Commands from the brain, traveling along a motor nerve, reach a muscle. The muscle, in response to the commands, uses stored energy to contract: to become shorter. When the muscle shortens, one part of the skeleton moves with respect to another, and the animal moves in some way. A cheetah sprinting in pursuit of a gazelle, a bumblebee flying over a meadow to land on a flower, a great blue heron stabbing at a fish, bullfrogs calling, crickets chirping, Hillary Hahn playing the Bach D minor Ciaconna; all are the outcomes of patterns of muscle contraction.
We have only a dim understanding of the complex mechanisms by which a brain decides which commands to issue from moment to moment. However, biologists are certain about the design features that they expect – the general decision-making rules that brains use. Behavioral biologists assume that brains are organized so that from moment to moment, individual animals act as if they are asking themselves the following question: “What should I be doing at this moment to maximize my lifetime reproductive success?” In the past twenty years we have learned that animals in nature really do act this way. But to accept this premise, must we conclude that animals consciously make decisions and are capable of the mathematics, or at least the complex reasoning, required?
In the late nineteenth century, Wilhelm von Osten startled the public and professional psychologists by showing that his Arabian stallion, Hans, could perform arithmetical calculations, including addition, subtraction, multiplication, and division using integers or fractions, take simple square roots, tell time, read, and spell. Von Osten put questions to Hans either orally or using a blackboard. Hans repeatedly pawed with a forefoot to indicate the correct answer. Von Osten: “Hans, what is the answer to 10 divided by 2?” Hans paws five times. Von Osten was convinced that animals have mental capacities that are essentially equivalent to those of humans, and he toured with Hans to prove this point. A panel of experts convened and concluded that no trickery was involved.
Then a student, Oskar Pfungst, arranged for questions to be put to Hans when neither the questioner, nor anyone that Hans could see, knew the answer to the question. In these trials, Hans could not provide the correct answer. Pfungst noted that when Hans, pawing with a forefoot, approached the correct answer, von Osten and others performed very slight, almost unnoticeable movements, such as raising or lowering the head by a fraction of an inch, or making tiny changes in facial expression. At the moment that Hans reached the correct answer, the release of anticipation in the human created a tiny twitch or jerk. What Hans had really learned was not math, but that in order to get von Osten’s training rewards, he should start pawing in response to the postural cues that accompanied a question, slow his pawing when subtle postural changes indicated that he was near the answer, and stop pawing when he observed the little movement that indicated release of tension in the human. Pfungst had discovered the phenomenon of unintentional cueing, which modern experimental psychologists call the Clever Hans Effect, and assiduously avoid in their experimental designs.
There are several lessons embodied in the story of Clever Hans. One, relevant to this chapter, is that animals can act as if they have complex contingencies in mind, and have conscious goals. Hans acted as if he could perform arithmetic, when the mechanism underlying his performance was simpler. A housefly can act as if she is constantly thinking about what she should be doing from moment to moment to maximize the lifetime number of her eggs that hatch, when her brain is far too small to produce anything like conscious thought.
In 1973, the Nobel Prize in Physiology or Medicine went to three European biologists: Konrad Lorenz, Niko Tinbergen, and Karl von Frisch. These men received the prize not only for the significant insights and discoveries that each had contributed, but also because they were leaders in a new field of biology: ethology. The Nobel Prize affirmed that ethology represented a significant intellectual shift – one might even say a thought revolution – in biology. What was the nature of the shift? It was that the behavior of animals was a proper subject for biological study. In other words, just as one may study a species’ skeleton, or organs, or muscles, so one may study a species’ behavior. There is a biology of behavior.
The thought revolution came from a deceptively simple technique – watching animals – but watching animals for long periods of time with patience, unwavering focus, and a willingness to suspend interpretation. When you watch an individual animal in this way, you begin to see that behavior is not continuous improvisation. There are repeating units.
The ethologists referred to these repeating units as Fixed Action Patterns. The designation “fixed” meant that the movement in question had the same form every time that it was performed. “Same form” means two things. First, if we describe the movement using technology such as slow motion video analysis, we see that the duration of the action, the sequence of flexion or extension of joints, and the degree to which each joint is flexed or extended, is identical every time that the action is performed. Second, and more fundamentally, the sequence and duration of individual muscle contractions is the same each time. We can discover whether this is so using a physiological technique called electromyography (EMG). When a muscle contracts, a weak electrical event sweeps across its surface. By attaching electrodes to the muscle, we can monitor when it is contracting and how forcefully it is contracting.
Any motion that you or any other animal performs is the result of a closely coordinated sequence of contractions of individual muscles. For example, just before you noticed the fly descending to your table, you raised the coffee cup to your lips, tilted it, and introduced some coffee into your mouth. Then, quite unconsciously, you moved the liquid in your mouth to the back of your throat, across the top of your windpipe, and into the top of your esophagus – you swallowed. That motion, swallowing, involved a precisely timed sequence of contraction of about a dozen separate muscles in your throat. Had one of the muscles started to contract one-tenth of a second too early or too late, the smooth movement of coffee into your esophagus would not have occurred.
Consider another famous Fixed Action Pattern made famous by ethologists – egg rolling. This motor pattern exists in a number of waterfowl species. Picture a goose parent, incubating eggs on a nest. Now we place an egg or an egg-shaped object in front of the nest. The parent may have been looking to the side, but it suddenly turns to stare directly at the egg. For the moment, the egg claims all the parent’s attention. After a few seconds, the parent stretches its neck forward, places its bill over the far side of the egg, and tucks its bill toward its chest, drawing the egg into the nest. The action obviously evolved because parents that retrieved wayward eggs back into the nest left more surviving offspring than parents that did not. A variety of objects will suffice to initiate this motor sequence in an incubating parent, and once initiated, the action runs, machinelike, to its conclusion. One can even reach in and remove the egg – the parent will continue with the tucking motion as if the egg were still present.
The extraordinary feat of the ethologists was that they did not reach their conclusion about repeating units of behavior with slow motion analysis or EMG. They simply watched animals with enough attention to perceive this truth. They also realized that one could compile a catalog of all the action patterns in the repertoire of a species. The term that emerged for such a catalog was “ethogram.” An ethogram for a species comprises a short descriptive phrase to denote each action, accompanied by a succinct description of the movement, for all movements performed by the species.
As ethologists continued to construct and to refine ethograms, they realized that not all motor patterns were as lengthy as egg rolling. However, the longer duration motor patterns were an entry point that allowed ethologists to appreciate that behavior is composed of fixed, repeating units. This fundamental insight has held up for over half a century. Today, there is some debate over the nature of the indivisible units, but little debate over their existence.
Another fundamental insight emerged from the construction of carefully conducted ethograms in an increasing number of species. This was that patterns of similarity and difference in ethograms mirror evolutionary relatedness. If two species have recently diverged from a common ancestor, the lists of motor patterns of the two species will be similar and the individual motor patterns will be similar in form. For example, humans and chimpanzees are closely related and they have similar ethograms. Both species laugh. Both beg by holding out a hand, palm up. In contrast, if two species are not closely related, then their ethograms are dissimilar.
That patterns of similarity and difference in ethograms match patterns of phylogeny (evolutionary relatedness) was powerful evidence that the ethologists were correct in their assertion that behavior is part of a species’ biology. It was already widely known, from Darwin and earlier biologists, that observed patterns of anatomical similarity and difference corresponded to phylogeny. The ethologists of the first half of the twentieth century figured out a way to describe the “anatomy” of behavior and found the same pattern. Motor patterns are gained, lost, and modified within any evolutionary lineage of animals.
Beyond Ethograms – Tinbergen’s Four Questions
In a now famous 1963 paper, Niko Tinbergen, who would share the Nobel Prize ten years later, outlined his thoughts on how ethologists should set research goals after they had learned to describe behavior using ethograms. Tinbergen had two main goals for his essay. First, he wanted to give full credit to Konrad Lorenz (another of the 1973 Nobel Laureates), who he considered to be the father of modern ethology. Lorenz, more than anyone else, should be recognized as the principal champion of the view that behavioral traits were biological traits. Second, Tinbergen argued that to fully understand any motor pattern, one needed to amass knowledge about it in four domains. We now refer to these as Tinbergen’s four questions. The domains, in the order listed by Tinbergen, are:
This domain embodies two sorts of information. First, what external stimuli are necessary and sufficient to elicit the motor pattern? For an incubating goose, we know that the stimulus needed to elicit egg rolling must be essentially egg shaped, and we know that a larger than normal egg-like object is even more effective than a true egg. By experimentally altering the nature of the “egg” that we present to the goose, we can discover the precise aspects of a stimulus (the ethologists used the term “sign stimulus”) that turn on (the ethologists used the term “release”) the egg-rolling motor pattern. Second, what is the nature of the “wiring diagram,” the brain architecture, that identifies the stimulus, makes the decision to turn on egg rolling, and issues the specific commands to muscles? For all but the simplest behavioral acts, we have only vague answers to this set of questions. Even for a housefly, the switching mechanisms that direct movement from one moment to the next are hideously complicated.
Next, Tinbergen turned to a domain that was controversial and little studied at the time: how a behavioral act contributes to the survival, and ultimately to the reproductive success of the animal that performs the act. When Tinbergen wrote his paper, many biologists thought that study of the function of behavior (how behavior contributes to survival and reproductive success) was not possible. Tinbergen pointed out that patient observation of animals in nature leads to hypotheses about function.
First, as one becomes better acquainted with a species, one notices more and more aspects with a possible survival value. It took me ten years of observation to realize that the removal of the empty eggshell after hatching, which I had known all along the black-headed gulls to do, might have a definite function… (Tinbergen, 1963, p. 422.)
Further, Tinbergen showed, in pioneering studies, that experimental tests of these hypotheses could be conducted in nature. He tested the hypothesis that eggshell removal by gull parents contributed to the survival of young by scattering gull eggs in an area where bird predators of eggs hunted. He placed empty eggshells near some of the eggs, and showed that predators found these more quickly than the eggs with no eggshells nearby. Field tests of hypotheses about the function of behavior constitute the majority of research done in animal behavior today.
Ontogeny means development. Here, Tinbergen applied his characteristic lucidity to a vexatious issue – the nature–nurture debate. In the 1960s, this was essentially a European–American debate. The European ethologists, with a tradition of observing animals in nature, contended that many behavioral acts, such as egg rolling, were instinctive, or “innate.” The acts appeared in perfect form the first time that the animal perceived the appropriate stimulus. American psychologists, in contrast, had a rich tradition of experimentation and careful consideration of experimental design, using a few domestic species (mainly Norway rats, house mice, and pigeons) in controlled laboratory settings. The Americans contended that many, if not all, behavioral acts were influenced by learning. Thus, a contentious transatlantic debate arose on whether motor patterns were instinctive or learned.
Tinbergen pointed out that the debate as framed was not useful. He noted that labeling an act as either instinctive or learned is to make a claim about the role of experience in the development of the act. Labeling an act as instinctive implies that the act develops with no experience of any sort required. But, Tinbergen argued, proving that no experience is required means that we must experimentally prove that each independent possible source of experience is not needed: ultimately, we are faced with an almost endless number of negative proofs. A complementary difficulty arises when we want to claim that an act is learned. Tinbergen argued that, rather than labeling an act as instinctive or learne...