Introduction

This short review is intended primarily as an introduction for students not acquainted with the literature of ethology. Within the space available it has been necessary to be selective; I have attempted at least to mention all the major aspects of the subject but it has not been possible to give equal attention to them. My personal interests and opinions have no doubt introduced some bias and placed emphasis where others would not put it. For this I make no apology.

I have chosen to treat the subject in a roughly historical fashion: firstly because in a short period ethology has undergone such rapid development that it already serves as a good example of how sciences progress; secondly because some of the older ideas of ethologists are still in current use in some quarters, although they have been superseded in the opinions of most present day workers. I think the newer ideas can be best presented by indicating how they grew out of the older.

Thesis

By and large the psychologists had looked for behaviour, in animals, that conformed to the categories of learning patterns that had been worked out for humans, and had found little else^*; or they had dismissed the possibility of a satisfactory analysis of animals other than humans because such animals cannot introspect and tell us about their motives (e.g. Bierens de Haan, 1947). The physiologists, working at the level of simple reflexes, had generalised their results to the point of saying that all behaviour can be reduced to description or explanation in terms of simple stimulus-response connections — nervous links between specific receptors and specific effectors (e.g. Pavlov, 1927).

It was largely a reaction to these teachings which established the existence of ethology. Konrad Lorenz (e.g. 1935, 1937 a & b, 1950), building on the work of such people as C. O. Whitman, Oscar Heinroth, Wallace Craig. Edmund, Selous, Eliot Howard, Julian Huxley and Jan Verwey, showed that the doctrines of Gestalt or ‘purposivist’ psychology (the European school that denied the possibility of behaviour analysis without introspection), and of behaviourism (the composite of learning theory and Pavlovian reflexology that flourished in America during the thirties) would not do when applied to the majority of animals in nature. The Gestalt people were convicted of vitalism, of retreating into mysticism before the limitations of a scientific analysis had been tested. The behaviourists were praised for their tough-mindedness but censured for their narrow-mindedness. If they had taken the trouble accurately to observe their animals, Lorenz claimed, they would have seen that much of the behaviour was spontaneous — not dependent on changes in the immediate external stimuli — and that reaction to a stimulus was rarely constant. The facts, for Lorenz, indicated a measure of internal control that is independent of the external stimuli of the moment. A further set of facts indicated that certain aspects of this internal control are independent of the stimuli of any moment, i.e. they are inborn rather than acquired by experience — innate rather than learned.

Properly to understand a piece of behaviour we have to appreciate its function in the life of the animal and its position in the whole behavioural repertoire of the animal. This necessitates study of the animal in its natural situation or in conditions that do not disguise the biological relevance of its behaviour. Studies of this

Finally there were observations of animals performing complicated behaviour patterns perfectly at the first opportunity without previous experience of practice or imitation. For example Grohmann (1939) reared a group of pigeons in narrow tubes so that these birds were prevented from carrying out the flapping movements of the wings which young pigeons perform before they can fly. At the age when pigeons are normally able to fly these experimental birds were released and flew immediately as well as unconfined controls. A similar experiment was carried out by Spalding (1873, 1954) on young swallows. Carmichael (1926, 1927) raised a number of tadpole eggs in a solution of chloretone, a substance that produces anaesthesia of striped muscle but permits normal growth. This prevented the practice of swimming movements by the developing tadpoles, but when they were eventually placed in pure water they swam as prefectly as controls of the same age that had been reared in normal conditions. To this list could be added the cases where trial and error learning is ruled out because unless a response is performed perfectly at the first time of asking, the animal is killed. For instance, unless the courtship dance of a male salticid spider inhibits the feeding responses of the female, he will be killed and eaten at his first attempt at mating. These cases, Lorenz argued, could not be explained as instances of learning from experience in the life of the individual; they could be explained only in terms of the history of the species and its genetic endowment.

The writings of Lorenz stimulated field naturalists and zoologists to pay close attention to the behaviour of animals and to think of it in terms of biological function and evolutionary origin. Detailed descriptions were produced such as the ethograms of Makkink (1936, 1942), Tinbergen's studies of birds (1935, 1939), insects (Tinbergen et al, 1942), and fish (Ter Pelkwijk & Tinbergen, 1937), Baerend's work on digger wasps (1941) and cichlid fishes (Baerends & Baerends van Roon, 1950). The functional significance of such things as the bill colour of gulls (Tinbergen, 1949. Tinbergen & Perdeck, 1950), countershading in caterpillars (de Ruiter. 1955), the red breast of the Robin (Lack, 1943), the page 174 large cheliped of male fiddler crabs (Crane, 1941), and the eye-spot patterns on the hind wings of Lepidoptera (Blest, 1956) were demonstrated by observations and experiments on behaviour. Comparison between related species indicated ways in which behaviour evolves, e.g. Tinbergen (1952, 1954), Daanje (1950). Behavioural characters were found to be useful in working out taxonomic or phylogenetic relationships (e.g., Lorenz, 1941, Spieth, 1950) and were sometimes even superior to structural characters in this respect (e.g. Adriaanse, 1947, discovered, on the basis of clear differences in behaviour, that what had been judged as a single species of digger wasp, on morphological grounds, was, in fact, two distinct species). New information was accumulated about the sensory worlds of different kinds of animals and their roles in the control of behaviour patterns (e.g., see Tinbergen, 1951).

As further support for his belief that much behaviour is the expression of endogenous co-ordination and energy fluctuations, independent of afferent input, Lorenz cited the work of von Holst, Weiss and W. R. Hess. Von Holst (1932, 1933) had shown that the isolated nerve cord of an earthworm, deprived of all afferent stimulation, continues to send vollies of impulses along its length and that the timing of these rhythmical vollies corresponds exactly to the contraction waves that pass down the segments in normal locomotion. A spinal eel with its nerve cord isolated from all proprioceptive input continues to perform perfectly co-ordinated swimming movements (von Holst. 1937). In experiments on the growth of nerve fibres in axolotls. Weiss (1941) contrived a transplated limb graft that received connections with motor nerve fibres from the nerve cord before it had received any connections with sensory fibres; such a limb graft began making perfectly co-ordinated walking movements as soon as the motor nerves made their connections. Hess (e.g., 1956) electrically stimulated the mid-brain of cats with implanted electrodes and found that it was possible, by this means. to produce fully co-ordinated behaviour patterns, including appetitive sequences terminating in consummatory act, identical with normal behaviour. In Lorenz's view such experiments as these could not be accounted for by a chain reflex theory of integration.

Lorenz's scheme was elaborated by Tinbergen (e.g. 1951). He gave a more neurophysiological ring to it by renaming the action specific energy as motivational impulses and by referring to the sources of these impulses as centres in the central nervous system. Tinbergen (1942, 1950) and Baerends (1941) also introduced the notion of hierarchy into the system. Behavioural functions can be classified in a hierarchical fashion. An act can be described as belonging to a series of progressively more comprehensive classes. For instance a particular movement might be labelled as ‘digging’; this, together with others such as carrying material, will be further classified as ‘nest building’; nest building, together with classes on the same level such as courtship, territorial fighting, care of offspring, can be classed together as reproductive behaviour. Tinbergen claimed that the course of many behavioural sequences is a descent through such a hierarchy of functional classes. To return to an earlier example, the hawk that flies over the country is showing appetitive feeding behaviour; the precise behaviour that this leads to will depend on the kind of stimuli that is discovered — if the hawk encounters a flock of small birds it will do one thing, if it encounters a lone pigeon it will do another, if it sees a young rabbit will do a third thing. Whatever the kind of prey encountered, the result will be a switch to a more restricted class of actions (‘starling catching’ behaviour for example). Once the prey is secured the new set of stimuli at page 177 the bird's disposal guide it into the still more restricted classes of acts involved in killing, plucking and dismembering, and this finally provides the stimuli which release the fixed action pattern of the consummatory acts of biting-off and swallowing. Tinbergen represented his scheme graphically as a set of centres each of which was controlled from above by supply of motivational impulses, and from below by an IRM which could be opened by the action of a small range of external stimuli. The sequence of releasing stimuli encountered progressively narrowed the choice of outlets for a stream of impulses as it descended from level to level down the hierarchy of centres — the animal proceeds to more and more restricted types of appetitive behaviour until the sequence terminates in the end act.

A prominent place was given to innate elements in these theories. It was believed that learning could affect appetitive parts of a behaviour pattern to some extents but the consummatory act was regarded as purely innate — its constancy of form in the life of the individual, and in each individual of the species, pointed to the stability of species genotype rather than the uncertainty of environmental influences. The releasing mechanisms were labelled as innate for the same reasons.

Lorenz emphasised that learning could, for particular behaviour patterns, be confined to crucial short periods during development. He (e.g. 1935) found that in many birds, such as ducks and jackdaws, if the young are exposed to certain stimuli during a critical period in early life, these stimuli become irreversibly linked to certain behaviour patterns. Thus a duckling can be made to treat a green box as if it were its mother, and a jackdaw can be made to direct all its courtship behaviour to a man. This phenomenon Lorenz called imprinting.

Ethology, then, in the early 1950s, could be identified with a school of animal behaviour students who approached behaviour from the direction of ecology, evolution, taxonomy and comparative anatomy; who consequently emphasised the roles of genetic components in the development and control of behaviour; who insisted on thorough study of the whole of an animal's behavioural repertoire, preferably in its natural setting, and developed a set of new technical terms for classifying and describing behaviour; and who interpreted their findings in terms of models of energy generation, flow, accumulation and exhaustion.

These models exerted considerable influence and still provide the conceptual basis for analysing and thinking about behaviour in some quarters. They had the virtue of introducing order into a wide range of otherwise unconnected facts; their elegance and comprehensiveness carried considerable appeal of a sort that might he called aesthetic.

(To be continued)