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Tinbergen�s Four Problems - where are we now?

Greg Detre

Wednesday, 25 April, 2001

Prof. Steve Simpson, Natural History Museum

Ethology can be most simply described as the science of animal behaviour. This extremely broad definition immediately raises questions about where boundaries with related disciplines lie. Tinbergen�s famous 1963 article, �On aims and methods of Ethology�, consolidated and redirected ethology along four broad lines: causation, survival value, ontogeny and evolution. His guiding aim was to reform Ethology as �the biological study of behaviour�, following the general approach of his mentor, Konrad Lorenz, in seeing a behaviour as an �organ� much like a physiological organ. Since Tinbergen�s seminal paper, a plethora of revisions to his framework have been suggested, and the status of the discipline of ethology relative to physiology, psychology and neurobiology (among others) has altered. Following Tinbergen, I will discuss the Four Problems as he set them out, and then try to consider alternatives, criticisms and the wider perspective after.

Firstly though, it may be important to consider what is meant by �behaviour�, given its central position in ethology. The most basic starting definition is �Behavior is motion.� When Tinbergen describes his over-arching discipline of the �Physiology of Behaviour� as the �study of causation of animal movement with respect to all levels of integration�[1], he appears to be adopting this stance. Unfortunately, behaviour as motion ignores many types of behaviour, such as the fright response and sleep. A more adequate definition is: �What a plant or animal does, in the course of an individual's lifetime, in response to some event or change in its environment.� (Silvertown, J. and Gordon, D. M. A framework for plant behavior. Ann. Rev. Ecol. Syst. 20:349-366, 1989). This probably includes everything that we would want �behaviour� to include, but may be a little bit too general. Rather, �Behavior is all observable or otherwise measurable muscular and secretory responses (or lack thereof) and related phenomena in response to changes in an animal's internal or external environment." (J.W. Grier and T. Burk, Biology of Animal Behavior, 1992). This definition outlines what sort of physiological mechanisms we mean, while remaining satisfyingly broad, and should be suitable for our purposes.

Tinbergen advocates Lorenz�s approach of treating behaviour as an organ, admissible to the same biological method, and similarly unsuitable for �subjectivist� accounts (i.e. those which rest on a highly anthropomorphised view of the animal�s mentality, or apply folk psychological explanations like �the animal attacks because it feels angry�). He also advocates caution in how we name complex groups of behaviour, such as nest-building, fighting or sexual behaviour. Terms such as these relating to major functional units are often confused as units of mechanism; no physiologist using the term �eye� to apply to a vertebrate lens and also a compound Arthropod eye assumes that their mechanisms are the same, but only that their function, or achievement, is comparable. By treating behaviours as organs, we stress to ourselves that every animal has a varied and extensive arsenal of behaviours, just as our body harbours many organs, but that these remain largely constant and fixed across a species, ceteris paribus.

Tinbergen raises an important point in his discussion of causation, about the respective places of ethology and neurophysiology, or neuroethology as it is now known. At the time he was writing, the techniques available to neurophysiology limited its investigations to the very basic and low-level, and were insufficient to analyse the complex behaviours that ethology addressed. As he foresaw, both disciplines have increased the scope and power of their analytic techniques in the intervening years.

However, M. S. Dawkins (1989) points to a very different and equally worrying issue in modern ethology. Tinbergen�s article directly guided the activities of a generation of ethologists, now considered �classical ethology�, where the adaptiveness of a behaviour was under-studied. On the other hand, modern ethology has emphasised evolution and adaptive function at the expense of mechanism. Tinbergen showed, with his characteristic attention to experimental detail and observation, how studies of adaptive function can be carried out in order to draw legitimate conclusions, but this rested on a firm body of work carried out on the mechanics (or �causation�) of the behaviour in action. As Dawkins readily admits, an imbalance in the opposite direction, favouring mechanism over evolutionary explanations, would prove �dry and dusty�. She argues vehemently for a redress, since ethology functions most healthily when it keeps all four of Tinbergen�s problems in perspective.

Tinbergen pays repeated tribute to Lorenz�s interest in both �What is this good for?� and �How does it work? when discussing an organ (with an �organ� being characterised by its function). Here, Tinbergen draws an important distinction between experimentation into the survival value (or adaptive function) of a given organ exhibited in the present, which is open to scientific enquiry, and experimentation into the particular, contingent evolutionary history which has led up to the species� current state, which can only be �traced indirectly�. �Causation� seems a misleading name for the study of the mechanisms of an organ, given that Tinbergen wants us to view the causation surrounding the exhibition of a given behaviour in both directions: its mechanical/physiological cause(s), as well as its effect on survival value. Both are �observable aspect[s] of a life process�, and are �concerned with a flow of events which can be observed repeatedly and � thus � can be subjected to observation and experiment�, unlike the �events of past evolution�. In theory then, we are studying the causes of survival, but since in reality it is behaviour that we observe directly, we necessarily see everything from a behavioural perspective.

The problems of assessing survival value stem from the fact that behaviour is not a piece of matter, like a physiological organ, and usually we cannot simply excavate it, leaving the surrounding structures intact. At best, we can systematically compare the success of animals at times when they do and do not show a given behaviour, but we have to be extremely careful about the factors that we cannot control that may be influencing this. Tinbergen suggests the use of �dummies, which we can control.

The term �survival value� that Tinbergen used has since been largely replaced, in recognition of the need to emphasise the cross-generational consequences, rather than just the survival of individual organisms. As a result, �adaptive or biological function� are usually preferred. Pittendrigh�s (1958) use of �teleonomy� (�The property of living systems of being organized towards the attainment of ends without true purposiveness� - SOED) may have been apposite, but never caught on.

The major area of ontogeny (�The origin and development of the individual organism� - SOED) that ethology was focused on when Tinbergen was writing was that of learned vs innate behaviour (though he remarks that the opposite of �innate� is really �environment-induced�). His evocative example of why a young cliff-dwelling Gannet cannot learn to fly the way we learn to write highlights why ethology�s early investigations focused on innate behaviour. He defined �ontogeny� as �change of behaviour machinery during development�, in order to distinguish it from merely a cyclical or otherwise incidental change in behaviour. He was also keen that innateness be demonstrated negatively, that is, by elimination � only when no environmental or cultural influences that could have shaped the behaviour can be found, can we describe it as �innate�.

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Evolutionary study has two aims: trying to trace the path that evolution took, and understanding better how evolution affects behaviour. In the first case, treating behaviour as organs allows for semi-quantitative comparisons between different species, to see how much they differ and so when their evolutionary paths probably diverged. In these studies, correlations with taxonomists� techniques are apparently good. The second task is closely related to assessing survival value, and indeed the two areas inform each other.

Tinbergen�s outline of the ethology�s investigation into evolution was deficient in one prominent area. Hailman and others have deliberately chosen or extended this area to explicitly incorporate non-genetic cross-generational transmission, usually in the form of cultural heritage. Hailman�s chosen term was �phylogeny�, in its broader, original sense. This provides a neat complement to �ontogeny�, but is frequently misunderstood due to his slightly unusual, technical usage.

It remains to clarify the proximate-ultimate distinction. Dewsbury (1992) discusses the pitfalls inherent in the word �ultimate� (rather �distal�, which is the more typical complement of �proximate�). �Ultimate� signifies distance, but also something more fundamental, leading to a confused hierarchy of levels, which Tinbergen had been explicitly keen to avoid. As Francis (1990) puts it, �Granted, �distal� lacks some of the connotations of �ultimate�, but it is meaning well lost�.

Baker�s (1938) and Lack�s (1954) usage aligned this proximate-ultimate divide with a how-why divide. In this way, proximate (i.e. immediate) explanations deal with the mechanics of how an action can be explained, usually in physiological terms, and ultimate explanations point to the macroscopic factors influencing the action, usually evolutionary. Mayr (1961) took this further, linking proximate causes with individuals and organs, and ultimate causes the evolution of DNA codes.

It was only much later (Alcock, 1975), that �proximate� came to stand for causation and ontogeny in Tinbergen�s problems, and �ultimate� for function and evolution. When seen in this way, the proximate-ultimate distinction seems to be delineating the study of behaviour within an individual on the one side, and behaviour that transcends the individual on the other. Of course, even this analysis muddies things further, since survival value (Tinbergen�s term) is an issue for individuals, but the intergenerational adaptive function (Huxley 1942 and Hailman 1976) of a behaviour goes beyond the individual. This illustration only shows that such strict attempts at classification inevitably shoe-horn scattered areas of the discipline or split apart natural groupings. In the same sprit, Hailman�s (1976, 1977) double partitioning on the basis of individual/population and cause/origin splits Tinbergen�s four problems rather neatly into:

	Individual	Population
Causes	dynamic control	adaptive function
Origins	ontogenetic development	phylogenetic origin

This is probably as far as grouping of Tinbergen�s problems can be taken. Although the �origins� row works well, Tinbergen had been keen to view �function� or �survival value� as an effect, though of course he recognised that eventually every effect becomes a cause. Also, Tinbergen stresses the importance of considering the adaptive function of ontogenetic development, giving the example of young birds who will try and eat almost anything, learning whatever happens to be edible in the particular region they grow up in.

The status and pitfalls ethology is subject to have changed greatly since Tinbergen was writing, especially since Wilson�s (1975) �Sociobiology�. Tinbergen�s own emphasis on amassing a body of observational and experimental evidence upon which to firmly ground any discussions of ultimate is still relevant, especially since the study of evolution outweighs the other three �legs� of the ethology-animal (to use Dawkins� terminology).

However, in more than just the obvious sense, this entire discussion is academic. Dewsbury�s (1991) �Table 1� serves extremely well to highlight the fundamental commonalities between the various revisions and make-overs since Huxley and Tinbergen. These �areas� (Lehner, 1979) or �problems� come down to:

How do the (physiological) mechanisms underlying a behaviour work?

How does the behaviour develop over the lifespan of the animal?

Why does the animal perform the behaviour / What adaptive function does it serve?

How has the behaviour of the species evolved?

Tinbergen built on Huxley�s (1942) earlier tri-partite �aspects of biological fact�, adding ontogeny to the list, and making the structure famous and influential.� But in a way, such explicit formulations of the remit of a discipline are redundant. The dynamics of scientific disciplines, as they vye to survive the next funding round, their fitness ostensibly evaluable in terms of papers published and their complex interactions across a huge geography would make many University departments interesting organisms for study. Certainly, the ones still around have proved themselves remarkably successful at evaluating the direction of their discipline and, where necessary, repositioning themselves. Currently, the small handful of scientific disciplines have fragmented in every direction, possibly as a result of the need to specialise just in order to keep track of the volume of new material being produced. Ethology alone has become an inter-disciplinary meshing of neuroethology, physiology, psychology, cognitive ethology, philosophy of mind and artificial life. Though it helps to have explicit guiding principles and aims, ultimately ethology must follow the funding, which is ultimately influenced by commercial interest.