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Tuatara: Volume 12, Issue 1, March 1964

Ethology—The Zoologist's Approach to Behaviour — Part 2

page 16

Ethology—The Zoologist's Approach to Behaviour — Part 2

(continued from Vol. II, p. 177)


Beauty has been accused by being ‘only skin deep.’ The theories of Lorenz and Tinbergen soon came under attack from a number of directions and new facts began to accumulate which would clearly not fit the theoretical systems unless these were revised.

(a) Ontogeny

In the writings of Lorenz the impression conveyed to many was that behaviour was either innate or learned and that these classes were exclusive and exhaustive. At least he claimed that the essence of ethology was the discovery of ‘a distinct and particulate physiological process … a certain type of innate, genetically determined behaviour patterns’ (Lorenz, 1950: 221) which was independent of individual experience in the life of an animal. It was soon pointed out that there is a sense in which all behaviour is both innate and the product of experience — the outcome of interaction between inheritance and the environment in which the inherited material finds itself (e.g. Hebb, 1953). Tryon (1929) had already shown that learning ability has a genetic basis: from a single population of rats he selected pairs with similar maze-running performances and allowed them to mate. After several generations of such matings selected on the basis of maze learning he had two groups: one contained ‘maze-bright’ rats and the other ‘maze-dull’ rats and divergence between the two groups had reached the point where there was no overlap in maze running scores between them. On the other hand von Senden (1932) and Riesen (1947) had shown that an ‘inborn’ reaction could be dependent on prior learning to perceive certain stimuli. At a certain age chimpanzees show a fear response to snakes or snake-like objects. They show this reaction without any previous experience of snake-like objects or of opportunity to imitate the reactions of others to such objects. But the capacity to show the reaction is dependent on ability to perceive the object visually, and this ability is acquired through experience. page 17 Chimpanzees prevented from learning to see did not show the response when they had reached the appropriate age.

Beach (1955) complained that the crux of the definition of innate behaviour is that it (innate behaviour) is unlearned — a negative definition or definition by exclusion. Such a two-class divisions of behaviour is indefensible, Beach said, unless one is thoroughly clear about what constitutes learning and learned behaviour, and this no one could claim to be. Further, the confidence with which it is asserted that a particular behaviour pattern is innate tends to be inversely related to the extent to which the development of this behaviour pattern, in the life of the animal, has been studied. Lehrman (1953, 1955) made this same point by citing experiments which indicated the roles of interaction between organism and environment in the development of responses which, by all the standards accepted by the ethologists, would be classified as innate, e.g. the pecking of chicks (Kuo, 1932), the parental behaviour of rats (Birch, unpublished observations cited by Lehrman, 1955: Riess, 1949).

Lehrman (1953) and Schnierla (1956) made the further point that classification according to the innate-learned dichotomy tends to emphasise superficial resemblances at the expense of profound differences between different kinds of animals. For example Schnierla (1959) showed that ants and rats could learn to run the ‘same’ maze but that they went about the process in quite different ways. Moreover, whereas this experience tends to improve the rat's performances in subsequent encounters with new mazes, the ant performs worse, if anything, when it is given a new maze to learn. The apparent differences in the processes underlying the maze-learning of these two animals is masked by unqualified use of a blanket term to cover both. These workers warned that uncritical use of such question-begging terms as ‘innate’ and ‘learned’, when applied to events in the ontogenies of individuals, could act as a damper on curiosity — an invitation to consider a problem solved before it had been investigated*

(b) The consummatory act and appetitive behaviour

Although the distinction between ‘appetitive’ and ‘consummatory’ behaviour provided useful pigeon holes in the initial stages of descriptive ethology, it was soon shown to be a difference of degree rather than of kind, and that a number of

* It is a nice irony that Lorenz, who claimed that it was possible (let alone an ‘inviolable law’) for science ‘to begin with pure observation, totally devoid of any preconceived theory and even working hypothesis’ (Lorenz, 1950: 232), should be taken to task for selecting examples to demonstrate an a priori principle and for failure to take account of the facts because of rigid and preconceived ideas (Lehrman, 1953).

page 18 patterns, such as flight responses from predators, did not fit easily into either of the two categories (Hinde, 1953).

The notion of consummatory act was questioned when it was shown that the terminations of many behaviour sequences are not actions involving the expenditure of muscular energy, but situations which provide a specific pattern of stimulation (Moynihan, 1953; Bastock, Morris & Moynihan, 1954; Kortlandt, 1955, Hinde, 1954). The work of von Holst and his students (von Holst & Mittelsteadt, 1950; von Holst, 1954) introduced the concept of Reafferenz or negative feedback into ethological thinking. Roughly speaking the Reafference Theory says that a particular act is ‘ordered’ by the central nervous system with the ‘expectation’ (Sollwert) of a certain result; the stimulus changes effected by the performance of the act are fed back into the CNS and ‘compared’ with those expected. Subsequent action depends on this comparison: if there is discrepency between received and ‘expected’ stimuli further action is instituted in the direction which will correct the discrepancy, Von Holst and Mittelsteadt took as one of their examples the optomotor reflex of the house fly. If a pattern of vertical stripes is moved across a fly's visual field the fly will reflexly turn in the same direction as the moving stripes. When the fly itself moves and the stripes stay still the effect, as far as the fly's visual receptors are concerned, is again movement of stripes across the visual field, but in this case the turning ‘reflex’ is not shown. The reason given for this by classical reflex theory was that, when the fly moved, the turning reflex to moving visual patterns was inhibited. Von Holst thought there might be another explanation. If the fly's movements were affected by discrepency between ‘expected’ and received visual stimuli then the optomotor reflex might be absent when the fly moved because then the changes in its visual field were changes that it ‘expected’ to result from its movements. To test this hypothesis von Holst and Mittelsteadt rotated the head of a fly through 180° and glued it to the thorax so that its left-hand eye was now on the right side and its right hand eye on the left side. This meant that a stripe that was actually crossing the visual field from left to right seemed to the fly to be crossing from right to left. If the classic reflex theory held, this should make no difference to the fly's behaviour when it moved. In fact, however, whenever the fly moved, it very quickly began spinning in small circles and would go on doing this until exhausted, and this is according to the predictions of the reafference theory. Twisting the head of the fly had caused it to misread its visual information so that the movement it made to correct a discrepency between input and Sollwert made the discrepency worse instead, which re-stimulated the movement to give further augmentation of the discrepency, and so on in a never ending vicious circle. The reafference model is similar in principle to the servo-mechanisms page 19 of engineers — such self correcting devices as the automatic pilot of an aeroplane, the governer on a steam engine, or even the thermostat on a stove: devices which can be set to effect or maintain a certain state of affairs and react to any deviation from that state of affairs be acting to remove the deviation. A similar idea is incorporated in Cannon's principle of homeostasis and is illustrated by such things as the control of circulation and respiration.

The application of this sort of thinking to animal behaviour tended to change the concept of the end act or consummatory act in the direction of consummatory stimulus situation — the stimulus input cancelling further action of a certain sort*.

(c) Energy models and the concept of drive

With the change of emphasis from the action at the end of a behaviour sequence to the stimulus input, the idea of consumption of energy or exhaustion of motivational impulses, came to look out of place. Moreover some of these ideas were at variance with what was known about the functioning of nervous systems. By drawing analogies with hydraulic systems and electrical circuits, Lorenz and Tinbergen had been led to attribute properties to nervous systems which neurophysiology had shown they could not possess — to talk of ‘damming up’ of impulses, ‘sparking over’, accumulation and ‘consummation’ of energy, was to take little account of what was known about nerve impulses and the functioning of neurones and neuronal systems. These shortcomings were pointed out in a series of papers by Robert Hinde (1956, 1959, 1960b), in which he also showed the inability of the ethological models, and the notion of ‘unitary drives’ that went with them, to do justice to other facts. He showed, for example, that where a behaviour pattern could be measured in a number of ways — frequency of performance per unit time, intensity of performance along some scale, latency after presentation of stimulus, duration of performance, strength of stimulus required to elicit performance, strength of stimulus required to inhibit the reaction or release an incompatible reaction — there was often considerably less than complete correlation between the values of the different measures (e.g. Hinde, 1958). Such degrees of independent variability between measurable aspects of a behaviour pattern were difficult to reconcile with the notion that an account of performance of a behaviour pattern could be reduced to fluctuation in a single variable, the ‘drive’, level of ‘action specific energy’, ‘motivational impulses’ or

* In a recent discussion of the concept of consummatory act Sevenster-Bol (1962) has argued that if the term continues in use it should have no more than a descriptive sense — it can refer to the end act of a behaviour sequence without implying anything about factors or mechanism involved in the termination of the sequence.

page 20 what not. Further, the use of such terms had discouraged the making of important distinctions at the same time as it had made distinctions where there was little evidence to support them. As an example of the last point Hinde cited the distinction between motivating and releasing stimuli — between stimuli which increased the level of action specific energy (or motivational impulses, or drive) and stimuli which effected the release of this in action; many stimuli obviously serve both functions and there is no good reason to believe that the functions are separated inside the animal in the form of two separate mechanisms (Hinde, 1960b: 208). On the other hand the ‘drive’ is frequently called on to explain a variety of aspects of behaviour that there is good reason to suspect depend on a variety of factors: Lorenz's ‘action specific energy’ energises the behaviour (provides the fuel), determines the kind of behaviour shown, its directedness, its possible persistence after removal of the releasing stimuli, its termination, the variation in releasability of the behaviour with time. To take just one of these aspects; studies of the waning of responsiveness to repeated presentation of a releasing stimulus, or a constant stimulus, have shown that several processes must be involved. Hinde (e.g. 1960a) has studied the waning of the mobbing behaviour of chaffinches to repeated presentations of the appropriate stimuli and his analysis revealed several effects: ‘To account for all the characteristics of the waning, it is necessary to postulate very short-term (i.e. recovery after a few seconds), short-term (recovery after a few mnutes), and long-term (recovery after weeks) effects. Further, in each time range, the effects may be positive (leading to an increase in response strength) or negative (leading to a decrease), and may or may not be specific to the stimulus’ (Hinde, 1959: 136). Roberts (1962; cited in Hinde, 1959) has shown that waning of the withdrawal reflex of earthworms is effected by changes at a number of points in the sensory, internuncial and motor portions of the arc, and that the relations between these changes are not simple.

A further objection to the use of drive concepts is that frequently vagueness of definition and inconsistency of reference are barriers to clear thinking. Two writers rarely employ the term in the same sense, and even within a single publication one is likely to find the term sliding between two or more, sometimes incompatible, senses: ‘drive’ can refer to extraneural state or intraneural state or both together, it can refer to a mechanism or to a quantity of energy, to tissue needs or ‘deprivation interval’ or deviation from a homoeostatic level (see Peters, 1958, for a linguistic philosopher's critique of the uses of ‘drive’). The concept of instinct presents similar ambiguity; Tinbergen, in a recent discussion (1960: 191) pointed out four quite different meanings of this term and he probably could have added more.

page 21

To overcome the bad features of early formulations of drive concepts in ethology a conference of animal behaviour workers (Cambridge in 1949 — see Thorpe, 1951) recommended that Specific Action Potential(ity) (SAP) replace the older terms and that the reference of this term should be to the readiness to perform, or the probability of performance of, a particular behaviour pattern in a particular situation; it was to imply nothing definite about internal mechanisms but was to be an objective variable based on observed behaviour. As a counter to imputations of teleological thinking (Lehrman, 1953: 352) and vitalism (Kennedy, 1954), Specific Action Potential was offered as an ‘operational’ term — a concept defined solely in terms of observations and measuring procedures*.

The SAP concept acquired current usage. It is now more often referred to as tendecy. In principle its use signifies a quantitative aspect of a piece of behaviour, based directly or indirectly on past observation. For instance if it is said that in a certain situation an animal shows a strong tendency to flee (say), or shows a high fleeing tendency, this means that we think that the animal is very likely to flee and we make this judgment because the animal has frequently fled when observed in this situation in the past.

Now Hinde (1960b) has pointed out than an explanatory model can err in two directions: as already mentioned it can be misleading if it attributes unreal properties to the explicandum; on the other hand if its properties correspond too closely to those of the explicandum it fails to illumunate it. For a model to explain it must have a wider reference or information content than the phenomena to be explained (e.g. see Braithwaite, 1959: 302; Harré, 1960: 101-2), otherwise all we are given is simply a re-presentation or redescription of our puzzle. Similarly a

* In the language of MacCorquodale & Meehl (1948) the older notions of Action Specific Energy and Motivational Impulses were hypothetical constructs — terms that postulated the existence of entities not immediately available to observation — and they had been found wanting because the supposed properties of these entities were inconsistent with certain already known properties. SAP, on the other hand, was an intervening variable only; a term which linked independent variables (such as time) with dependent variables (such as response strength) without carrying any further meaning.

To illustrate this distinction consider an example from physics. By making simultaneous measurements of the current and e.m.f. in a wire we find that there is a regular relationship between these two variables: E ഗ I. We can express this relationship as an equation by adding a constant so that E = 1R, where R is our constant which we call the Resistance. This is Ohm's Law. So far R is defined solely in terms of E and I; it is an intervening variable that enables us to make an equation. If, now, we try to explain the relationship between current and e.m.f. by some such notion as obstruction to the flow of electrons, we give the term Resistance additional information content (surplus meaning) and to this extent it becomes a hypothetical construct.

page 22 statement that purports to offer an explanation of a phenomenon must, as a minimum requirement, refer to something outside that phenomenon. Terms that stick to the status of intervening variables are limited to the function of stating relationships between the variables they link. This is a useful and necessary function but the point is reached when one asks for the explanation of the relationship. Now a hypothesis is called for which fits the relationship into a wider field of knowledge. In framing such a hypothesis it may be necessary to posit the existence of, as yet, unobserved entities or relationships. Whether this is done well or badly only empirical tests will show, but the step to hypothesis is necessary if the understanding of the phenomenon in question is to be advanced.

Perhaps awareness of the necessity for an explanatory hypothesis to refer to something outside the explicandum accounts for some inconsistent use of the SAP or tendency concept and some circular argument that has resulted from such inconsistency. For example van Iersel & Bol (1958), in a study of preening in terns, use the concepts of tendency to approach the nest and tendency to withdraw from the nest and one assumes that what is meant when it is said that the tendencies are at certain levels is that the probability of approach is so and so and the probability of withdrawal such and such and that these are judgments based on past observation. But when these authors attempt to say why the probability of approach is so and so, and the probability of withdrawal such and such, the ‘explanation’ is usually in terms of approach and withdrawal tendencies. Clearly, for this to be of any use, the senses of approach and withdrawal tendencies, in the explanatory statements, must include more than they started out with. In the theoretical part of this paper it seems that the terms take on the properties of unitary drive factors although the nature of these added properties is not made explicit. Similarly the notion of inhibition, as used by van Iersel and Bol, seems to start out as an operational concept, grounded in the fact that two particular responses do not occur simultaneously, and then, later, is put to use to account for the fact that these two responses are incompatible. This type of argument occurs also in a recent treatment of displacement activities, by another member of the Leiden laboratory (Sevenster, 1961).

In practice, also, the concept of SAP or tendency is frequently taken to refer to a quantity that can be measured equivalently in a number of ways, with little attempt to test the correlation between these different measures. Thus van Iersel & Bol (1958) use a number of measures as equally good indicators of ‘incubation tendency’: ‘sitting tendency’, the landing distance after alarm, the readiness to depart at nest relief, the time a bird has gone without incubating. My studies of incubation behaviour in gulls page 23 (Beer, 1961) indicated that the value derived from one of these measures might well contradict the values derived from others. Hinde's criticisms of this feature of older unitary drive concepts still apply.

Similar jumps were made, in some of the older work, when it was assumed that all the responses serving a particular function are expressions of the same instinct. This was usually taken to mean that these responses were controlled by the same underlying mechanism or drive, from which it followed that they had a closer causal affinity to one another than any had to responses grouped in other instincts. Tests of this assumption have shown that a classification of responses according to the ends they serve need not correspond to a classification according to common casual factors (Beer, 1963, in press).

Confusion between the cause and goal of behaviour, between efficient and final causes, seems difficult to avoid, and is perhaps due, in part, to the fact that we account for our own actions by stating the ends we had in view when we carried them out. If used carelessly some of the technical jargon of behaviour studies can help this confusion rather than dispel it; when we meet terms like‘ expectancy ’ and ‘intention movements’ applied to fish or insects it is an easy step to anthropomorphic thinking. The term motivation has a number of connotations. It is derived, etymologically, from the verb ‘to move’ which has also given rise to ‘motor’ and ‘motive’. Both of these notions — the idea of something that drives like an engine, and the idea of the end in view of an agent doing or planning something — attach to the idea of motivation so that the study of motivation can mean the study of motives and the study of the physical and chemical mechanisms underlying behaviour. No doubt in some contexts this is a false opposition but most of the time it seems wise to observe and maintain the distinction between the causes and goals of behaviour (for another view on this question see Hinde, 1957).

The ethologist, with his zoological background, emphasises the role of natural selection, and hence functional adaptation, in the explanation of behaviour. This was and is an important and necessary emphasis, but it encourages the tendency to identify proximate causes with ultimate causes, to assume that because a certain set of responses has been selected because they together achieve a certain adaptive end, these responses must be controlled by a unitary causal mechanism inside the animal. For example the fact that a particular posture occurs in a situation where two responses are equally likely to occur (e.g. approach and withdrawal) is often accounted for by saying that the posture arises because of the balanced conflict of these two tendencies (e.g. van Iersel page 24 & Bol, 1958; Moynihan, 1955; Tinbergen, 1959.* This argument is sometimes supported by, or confused with, the contention that the behaviour is explained historically by conflict between two opposed selection pressures, one favouring coming together of the animals, the other favouring their staying apart (e.g. Tinbergen et al, 1962), and that the posture in question has been evolved as a ‘compromise’ solution. Again it seems to me that clear thinking will be achieved only when we can hold apart the functional or historical explanation on the one hand, and explanation in terms of proximate causal mechanisms on the other.

Towards and Away from Synthesis

‘It does not seem over-optimistic to suggest that ethology is now entering a period of rapid expansion — a process which may, however, require a thorough revision of some of the concepts which have grown up with it and seen it through its teething troubles’ (Hinde, 1956: 321). The results of criticism of the older ethological concepts and theory, and the accumulation of new data, have been revision of the concepts and theory, increase in the precision of statements, increase in the detail of descriptive analysis, and application of the techniques and ways of thinking developed in other fields. This, together with the steadily increasing numbers of students, in both America and Europe, applying themselves to study of animal behaviour, has meant that instead of the small, rather homogeneous group of investigators that assembled for the first international ethological conference, we now find ethologists to be a large ill-defined group within which there has developed a number of special interests and considerable differences of opinion on many points. There is no general adherence to a specific structure of theory, as there was in 1950; technical terms have been brought much more into line with those used in related fields such as physiology and psychology and there is increasing cross-fertilisation with these related fields.

Is ethology losing its identity as a separate field of study then?

* As I have tried to point out for similar cases, if ‘conflict’ here means simply equivalence of probabilities for the two tendencies then we are given no new information; if, on the other hand, it means something more than this, we are entitled to ask what this something is and what independent evidence there is or could be for it.

The term ‘conflict’ is particularly liable to cause confusion because there are at least four senses that it can have in such a context as territorial fighting: it can refer to the fact that two animals are clashing — we might speak, in this sense, of a conflict of interests; it can refer to the fact that two incompatible tendencies are equally aroused (e.g. the animal is equally likely to attack or flee) —a conflict of possible outcomes; it could refer to conflict between the internal mechanisms underlying the two tendencies (‘fleeing drive’ and ‘attack drive’); or it could refer to opposition of selection pressures in the evolution of the behaviour — conflict of functions.

page 25

Perhaps it is to some extent, but the many present-day developments are clearly continuations of the ways of thinking about animal behaviour that were pioneered by Lorenz, and within the diversity one can see a unity of approach or attitude that derives from a common background of general zoology: the animals are still regarded from the standpoint of natural selection, as creatures that can be understood only if seen against the background of their natural setting.

This attitude is most clearly apparent in the students who try to explain behaviour in terms of its function, or use behavioural data to help in working out the adaptive value of some feature of form or function. Tinbergen's attention has been devoted to this sort of problem in recent years. One of his students has worked on the question of why so many sea birds have white plumage: from a study of the feeding habits of the birds and the visual responses of fish to differently coloured models he showed that the whiteness of the birds is very likely an adaptation to a certain kind of fish-catching way of life (Unpublished work by Phillips cited to me in a personal communication by Dr. Tinbergen). Tinbergen and a team of co-workers have examined the question of why Black-headed Gulls carry the broken egg-shells from their nests after hatching (Tinbergen et al, 1962). In a preliminary study (unpublished) I had found that carrying of shells from the nest could be released by placing shells in the nests at any time during the breeding season (not just at hatching), and that the reaction was shown not only to egg shells but to a range of conspicuous objects. Tinbergen and his students systematically tested the responsiveness of the gulls to a wide range of objects and found two peaks in this range: the more conspicuous an object was against the background of the nest the greater its releasing value, and the more like a real egg shell it was the greater its releasing value. Real egg shells were better releasers than any of the other objects even though they were considerably less conspicuous than some of them. This suggested that two selection pressures have acted in the evolution of the response; one favouring responsiveness to conspicuous objects in the nest, the other favouring responsiveness specifically to egg shells. The first suggested a visual predator and there were several obvious candidates for this role in the region such as carrion crows and herring gulls. To test the possibility that removal of conspicuous objects from the nest is advantageous because such objects might catch the eye of an egg-predator, the following experiment was set up: a number of artificial nests were made outside the gullery and eggs were placed in these nests, some containing a conspicuous object and others not. After a time these nests were examined and it was found that significantly more of those containing a conspicuous object had been robbed of their eggs. This result confirms that page 26 gulls which tend to remove bright objects from their nests will, on the whole, raise more young than will gulls that do not. The eggs of gulls are also taken by mammalian predators such as hedgehogs and foxes which locate their food mainly by smell. This suggested that the feature of the real egg shell, in addition to its conspicuousness, which favours its quick removal from the nest, is its odour. Another set of artificial nests with eggs was set up but this time half the nests contained a freshly broken and unwashed egg shell, and the other half contained a freshly broken and washed egg shell, and this arrangement was left for one night. The result was that the eggs were found and eaten in a significantly higher proportion of the nests with unwashed (and hence smelly) egg shells. Again this confirmed prediction on the basis of the hypothesis that olfactory predation acts as a selection pressure.

This study illustrates how a question of the form ‘Why does the animal do so-and-so?’ can be put in different ways: it can be directed to the causes acting directly, here and now, to produce the behaviour and these can be divided into those external to the animal and those acting within the animal; it can be directed to the function served by the behaviour — in the natural life of the animal and this in turn leads to consideration of the evolutionary history of the behaviour; it can be directed to the individual history of the animal — how has this behaviour developed in ontogeny? In the egg shell study, investigation of proximate causes (external stimuli) led Tinbergen and his colleagues to reach conclusions bearing on the function of the behaviour and hence on its ultimate causes in the history of the species.

Other workers have directed their attention mainly to unravelling the organisation of proximate factors underlying behaviour and here we can make a division between those who are concerned to make correlations between external factors, physiological states or events and behaviour, and those who are concerned to work out the formal properties that any physiological mechanism must have if it is to account for a particular behaviour pattern. This division is not a hard and fast one; there are various combinations of method and interpretation. In the first group we should include, as ground floor members, the many descriptive studies that establish the quantitative and qualitative regularities of animal behaviour (e.g. Lind, 1959; Manley, 1960; Wickler, 1962). Then there are numerous studies of the effects of natural or experimentally induced differences in such things as the available external stimuli (e.g. Beer, 1961, 1962 a & b, 1963; Hinde, 1958; Lehrman et al, 1961), hormone levels in the blood (e.g. Warren & Hinde, 1959; Lehrman & Brody, 1960), tissue needs (e.g. Tugendhat, 1960a), previous experience (e.g. Tugendhat, 1960b). Notable combinations of observational and experimental techniques are to be found in the studies of ‘biological clocks’ (see Cold Spr. Harb. Symp. page 27 quant. Bio. 25, 1960) and studies of homing and navigation in birds (e.g. Sauer, 1961). A particularly important recent contribution that we might also include in this group is the work of von Holst and Saint Paul on electrical stimulation of the mid-brains of domestic chickens (von Holst & Saint Paul, 1958, 1960). By implanting electrodes in the hypothalamus of roosters and hens these workers were able to make the animals perform elements of various behaviour patterns by stimulating the C.N.S. electrically in different localities and with voltages of different strengths. By stimulating two places at the same time they were able to produce interaction effects between two different behaviour patterns, and by stimulating in the presence and absence of certain external stimuli they were able to show interaction between internal conditions and external stimuli. The results were elegantly interpreted in neo-Lorenzian terms although it is doubtful if this interpretation is as logically compelling as the authors would have liked it to be. Some features of the experimental technique were too crude for an accurate judgment to be made about the relation between the data and natural functioning. More precise investigations with electrical stimulation of the brain are being undertaken on herring gulls and ring doves by ethologists at Oxford.

In the second group of workers are first of all the students who have been influenced by Cybernetics and information theory — the models of animal functions, particularly the functions of the brain, that have been drawn up by making analogies with the operations of telephone systems and electronic computers (e.g. Wiener, 1948). By tracing the patterns of qualitative and quantitative relations between dependent and independent variables that describe a behaviour pattern, students such at Mittelsteadt (e.g. 1958) and Hassenstein (e.g. 1960) attempt to work out the range of formal models that would produce such relationships. If these models are genuinely different they will lead to different predictions, and testing of these predictions should eventually eliminate all but the only adequate model. The best known and most accessible example of this type of thinking in ethology is still the Reafference Theory (von Holst, 1954) I mentioned in the last section. Such formal or mathematical models for behaviour tend to remain untranslated into terms of flesh and blood. Until they can be their heuristic value is probably limited.

A second approach to a formal model of the underlying organisation of a behaviour pattern has been by way of statistical methods. The increasing availability of electronic computers and data recording devices has allowed the analysis of a great deal more of the detail of behaviour patterns than was possible in the past, and also more comprehensive statistical treatment of such data (see Beer, 1962c). By application of the techniques of multiple correlation analysis and factor analysis it has been possible, in page 28 a few studies, to reduce the variations in a large number of variables to correlation with variation in a much smaller number of variables (see Wiepkema, 1961). Reduction to such independent variables offers the possibility of refinement in the definition of tendency with respect to a particular behaviour pattern: if a tendency is identified with one of these variables it remains an operational concept but, at the same time, makes more profound conditions about the properties that a physiological model for the underlying mechanism of the behaviour should possess.*

The study of the ontogeny of behaviour has not received the attention that one might have expected from the emphasis that was placed on the innate elements of behaviour in the earlier ethological writings. Tinbergen (e.g. 1955: 102) now admits the term ‘innate’ to be useful only when applied to differences in behaviour between animals (the differences in behaviour between identical twins are clearly not due to differences in genetic factors) or between species (the differences between a man and an ape are clearly not due only to differences in up-bringing) and not when applied to processes of development which give rise to behaviour patterns in the life of an individual. However Lorenz has recently published a rather polemical paper (Lorenz, 1961) in which he defends his dichotomy between innate and learned behaviour and ridicules ‘many modern ethologists, mainly those publishing in English’ who have not had the courage of their convictions. There is little that is new in his arguments except perhaps his

* Although the use of electronic recording devices and computers increases the accuracy and detail of description immensely it has not removed the element of arbitrariness that enters into any analysis of behaviour. Measurement involves the division of behaviour into units that can be counted or timed. Behaviour is a continuum that can be broken up in an infinite number of ways; every classification, of necessity, ignores some ranges of variation — the notion of a complete description is really a contradiction in terms. The selection of units for measurement will not be made at random; there will be some prior idea of what is useful or relevant to the problem on hand. But here there enters a danger if one is not self-critical of one's criteria of selection; it is possible to ensure that you get the answer you expect or hope for by unwittingly sorting the information to that end. If, for example, you want to know how often two postures are associated and you find that one of these postures occurs in a number of situations that seem to have nothing to do with the other posture you might want to leave the latter occurrences out of account. Unless you can find an objective way of making the separation into two classes of occurrences — one relevant and the other not — your result is likely to reflect no more than the association that you think ought to obtain between the two postures. Before units are selected for measurement it should be insisted that the student spend as much time as possible in familiarising himself with the whole behaviour of the animal, preferably in its natural habitat or under conditions which reproduce the essentials (a question-begging word!) of the natural situation. If this is well done the student will be in no doubt about the complexity of the problem with which he has to deal and he will regard his efforts at measurement with a healthy scepticism.

page 29 introduction of the concept of ‘information’. This is not defined with any precision but seems to mean something like ‘that which determines how a behaviour pattern develops’. According to Lorenz there are only two sources of such information as far as the individual is concerned: its genotype and its environment. Adaptedness between behaviour and the environment or way of life of the animal is obviously the product of natural selection and hence must be secured in the germ plasm. But this argument seems to be as far away as ever from helping in the understanding of the proximate causes or processes acting during the development of any piece of behaviour in an individual animal. The fact that adaptation must be secured in the germ plasm does not answer the question how adaptation is secured in the germ plasm in any instance. Perhaps Lorenz is not really concerned to ask such a question. But when he points out that for certain behaviour patterns to be adaptive they must be ‘environment resistant’, or for others that they must be performed perfectly at the first time of asking without prior experience of trial and error learning, and hence that the information for the developments of such patterns must reside solely in the genotype, he perhaps invites yet another confusion between ultimate and proximate causation — between the problem that was set by Nature and the nature of the solution in terms of the developmental processes in the individual. Further, the notion of information, as used in his paper, is so vague that in saying that the basis of adaptive responses must be genetically carried information Lorenz seems frequently to be saying no more than that the behaviour is the product of evolution, which surely is true of all behaviour in some sense. In spite of the suggestion of technical precision that it imports from the context of information theory, Lorenz's genetically carried ‘information’ seems to be little more than a blank cheque into which he can write any regularity which is species specific or species characteristic irrespective of the precise ontogenetic basis of such regularity. The translation of the ‘information rsquo; (whatever it is) into structure and function is a problem that cannot be decided in advance but can be worked out only by study of the development of individual behaviour patterns through ontogeny.* The arguments for ‘longitudinal’ studies of behaviour advanced by Beach (1955 a & b), Lehrman (1953, 1956) and Schneirla (1956)

* In a recent review Hess (1962) differs from me in being much more impressed by this paper of Lorenz's. We apparently differ also in our assessments of Hinde's examinations of unitary drive concepts; for Hess makes no reference to Hinde's papers on the subject, and uses the term drive throughout his review without any attempt to qualify its vagueness and ambiguity. I also object to his classification of Hebb, Lehrman, and Schnierla as ‘behaviourists’. This is either capricious or reflects profound misunderstanding of the work of these people.

page 30 remain as strong as ever. The practical problems involved in such study are often difficult and tedious but they are also exciting and important. Perhaps the chief merit of Lorenz's paper will be that it re-focusses some attention on this area of study.

The roles of experience in ontogeny have been extensively studied in the development of song in birds. This has been greatly assisted in recent years by the application of sound spectrography, a technique which enables one to get a pictorial record of sound as well as a measure of its frequency ranges. The consequent detail and precision of description and quantification are greater than is possible for most types of behaviour (see Marler & Isaac, 1960). By raising birds in isolation in sound proof conditions (what the Germans call the Kaspar-Hauser experiment) it has been shown that, with variations from species to species, certain features of a bird's song are affected by hearing the singing of other birds and other features are not (Thorpe, 1961; Blase, 1960; Thielke-Poltz & Thielke, 1960). A study of the ontogeny of responsiveness to a releasing stimulus, in birds, has shown that experience can be involved (Schaller & Emlen, 1961). Eibl-Eibesfeldt's (1956 a & b) studies of the ontogeny of certain behaviour patterns in mammals have shown that certain kinds of experience do not seem to be involved in the appearance of unit acts but that learning may enter into the linking of these acts into a functional sequence.

Imprinting has captured the attention of a number of ethologists; recent work in this field has been reviewed by Hess (1962). Hess's interpretation of the evidence is that the critical period is determined by the relationship between the development of locomotor ability and the development of fear of strange objects; when a certain degree of locomotion is possible, and fear responses are still relatively undeveloped, imprinting can take place. Sluckin & Salzen (1961) consider that imprinting is just a special case of perceptual learning. Hinde (1961) has pointed out that several different, although interrelated questions may be confused in these studies; of the tendency of a duckling to follow a moving object that it sees in early life it may be asked ‘Why does it follow?’, ‘Why does it learn to follow?’, ‘What limits the sensitive period?’, and ‘How does the early learning affect later experience?’ According to Hinde all of these questions are far from solution.

The influences of genes on behaviour have been demonstrated in studies of the behaviour of hybrids and also by selection experiments. Crosses between strains or species that differ in behavioural characteristics have produced hybrids that showed behaviour that was a mixture of that of the parents (e.g. Dilger, 1962, has crossed different species of lovebirds, Agapornis, and found that the hybrids showed ineffective combinations of the page 31 elements of the rather odd nest building techniques of these birds). Bastock (1956) has described a mutation which alters a behaviour pattern i Drosophila melanogaster. Mrs. Crossley, one of Bastock's students at Oxford, eliminated the progeny of all hybrid matings in a mixed population of two mutant strains of Drosophila and she found, after 40 generations of such selection against crossing, that the survivors showed differences in behaviour, between the two strains, that were not present in the original population, and that these differences were of the sort that would decrease the probability of crossing (personal communication). This result confirmed that of Knight et al (1956) who had shown that selection against hybrids between these two mutants resulted in progressive decrease in the numbers of hybrids produced from generation to generation; it also showed that anti-hybrid selection can result in the evolution of reproductive isolation of two strains as a consequence of changes in behaviour or responsiveness to stimuli (c.f. Mayr, 1942). These studies, of course, show only that genes are involved in the ontogeny of behaviour; they say little about how they operate in development or about the roles of organismenvironment interactions. Recent examples of comparative studies may be found in Tinbergen's review (1959) of the work on gulls, Andrew's review (1961) of hostile displays in passerine birds, and his study (Andrew, 1963) of the calls and facial expressions of primates. Wynne-Edwards (1962) has used behavioured data extensively in a new theory on the natural regulation of population densities and Klopfer (1963) has also recently applied a behavioural viewpoint to ecology.

The divergence of interests and methods that has developed within ethology has meant that in some parts of its range it has drawn closer to other fields of study. Concern with internal causes has resulted in liaison between ethologists and physiologists, particularly neurophysiologists and endocrinologists. Ethology now profits from developments in statistics and communications engineering. The traffic has not all been one way. Some of the generalisations that were made about behaviour on the basis of early discoveries in neurophysiology are now untenable in view of the work of ethologists. As psychologists and ethologists have come to realise that they have many areas of common interest, emotional and terminological barriers have given way to fruitful exchange of ideas. Ethologists are paying more and more attention to the discoveries, techniques and theories of psychologists (e.g. Hinde, 1959) and increasing numbers of papers by psychologists appear in the ethological journals and at ethological conferences. On the other hand the findings of ethology receive increasing attention in the writings of psychologists of all varieties (e.g. Carstairs, 1963; Gombrich, 1959) and ethologists are being appointed to the staffs of psychology departments at some American page 32 universities. References to the writings of ethologists have even crept into works of fiction (e.g. ‘Come Out to Play’ by Alex Comfort).


The most securely established achievements of ethology to date have been the precise and detailed descriptions of behaviour of a wide range of animals, discoveries of regular quantitative relationships between units of behaviour and between units of behaviour and other factors, recognition and experimental testing of adaptive functions of behaviour patterns and the use of behaviour in working out the adaptive significance of morphological features, recognition of behavioural homology and the use of this in working out evolutionary origins and in taxonomy. These achievements follow from the general zoological background of ethology: training in accurate and detailed observation, concern with comparative anatomy, with questions of phylogeny. adaptation, selection and ecology. It may well be that the future of ethology as a distinct discipline will also prove to be bound up with questions concerning what animals do and why they do it, in terms of functional adaptation, rather than in terms of causal mechanisms.

Explanation starts with generalisations based on observed regularities, e.g. the association of a particular environmental change with a particular response. But these generalisations explain their instances only to the extent that they can be derived from grounds other than just these instances. This usually means that such a generalisation is an instance of another more comprehensive or higher level generalisation, e.g. when we claim that a particular external stimulus causes a particular response we can appeal to the general principle that there are classes of events or things in the environment that can affect behaviour. This generalisation, in its turn, illuminates those subsumed under it only when it is related to an even wider field of knowledge, e.g., in our example, the relations between energy changes in an animal's perceptual field and events going on in its receptors. In the case of explanation of behaviour in terms of causal mechanisms the higher-level generalisations that we build into our pyramid of laws and hypotheses tend to be in terms of lower and lower levels of structure and function; we start with the whole animal and its environment, then go to stimuli and responses, then to the properties of the nervous system, or part of it, and so on. The problems sorted out by the ethologist at the level of overt behaviour will tend to be translated into problems about the fine structure and function of the animal body and hence to become the property of other specialists — the physiologists, embryologists, biochemists and biophysicists. The causal mechanisms propounded in some of the page 33 early ethological writings were unsatisfactory because they failed to take account of many of the relevant facts of neurophysiology; they were premature in that insufficient knowledge was available for the framing of connecting propositions between the generalisations of ethology and the generalisations of neurophysiology. In the absence of adequate knowledge of physiology, it seems that the elements of these hypothetical mechanisms were really drawn from the facts of behaviour; qualitative and quantitative regularities within and between functional classes of responses provided the only properties, of the causal models, which could stand empirical test (Lehrman, 1953, described these attempts to explain behaviour as ‘reifications’). This was recognised and made explicit in later writings by the reformulation of some of the variables in the older theories as operational concepts — terms the meanings of which were grounded solely in observations and measurements of behaviour. But statements containing no terms other these do not explain behaviour, they describe it or summarise it. When explanation is attempted with only statements of this sort we get either circular argument or the assumption of some unspecified reference outside the sphere of overt behaviour. Which ever choice is made we are likely to find that beliefs about proximate causes have been most strongly dictated by appreciation of the ways in which behaviour serves the biological functions of the animal. The zoological emphasis on the biological relevance of behaviour can mislead the ethololist when he moves from the description and measurement of behaviour, and the formulation of questions presented by such data, to the answering of these questions in terms of underlying causal mechanisms in the animal. Either he must acquire adequate knowledge of the ontogeny, physiology and fine structure of his animal, or he must hand his questions to someone who has such knowledge.

But questions about the proximate causation are not the only ones that can be asked about behaviour; equally important are questions about function, adaptation and evolution, and it is difficult to see how many of these questions can be translated into, or reduced to, questions of proximate causes. Indeed premature effort to make such translation or reduction could hinder our understanding of these questions rather than assist it. The kinetic theory of gases would not have been discovered if the behaviour of individual molecules had not been ignored in favour of the statistically probable behaviour of populations of molecules. The strength of Darwin's theory over those of his predecessors was that it showed the statistical implications of the presence of random variations in a population without, at the same time, trying to account for the origins of such variation (Gillispie, 1958). Similarly, if one accepts certain aspects of behaviour as given, one can page 34 attempt to account for the evolutionary history or consequences of such aspects by elucidating their functions and by comparisons between groups of animals with differing taxonomic affinities. Physiological considerations may enter at crucial points in such a study but, for the most part, quite different ways of thinking are necessary.

Recent advances in physiology, in biochemical genetics and biophysics, have produced a current fashion in favour of physicochemical explanation in biology. The history of biology shows oscillation between emphasis on low-level analytic studies on the one hand, and emphasis on high-level synthetic or ‘organismic’ studies on the other. Both of these viewpoints have their blind spots. Perhaps the present swing in favour of fine structure and function will be followed by renewed interests in problems peculiar to whole organisms or populations of organisms. In the meantime it would be unfortunate to lose sight of such problems. Ethologists are well placed to keep them in view.

Acknowledgment: I am grateful to Professor B. J. Marples for reading and commenting on the manuscript of this paper.


As introductory reading I recommend ‘King Solomon's Ring’ by Konrad Lorenz (Methuen, London, 1952). ‘Curious Naturalists’ by Niko Tinbergen (Country Life, London, 1958). As basic reading for a study of ethology I recommend ‘The Study of Instinct’ by N. Tinbergen (Oxford, 1951), ‘Learning and Instinct in Animals’ (second edition) by W. H. Thorpe (Methuen, London, 1963), ‘Instinctive Behaviour’ edited by C. H. Schiller (International Universities Press, New York, 1957), ‘Current Problems in Animal Behaviour’ edited by W. H. Thorpe and O. L. Zangwill (Cambridge, 1961), Symposia of the Society for Experimental Biology IV: Physiological Mechanisms in Animal Behaviour (Cambridge, 1950). A large proportion of the ethological work is published in three journals: Behaviour, Zeitschrift für Tierpsychologie, and Animal Behaviour (formerly The British Journal of Animal Behaviour).

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