Antithesis

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?

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 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).

Conclusion

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.