Animal Behaviour - Tinbergens Four Whys, Where are we now?

Ethology has developed considerably since early last century where it was regarded as a hobby for naturalists and animal keepers. It has developed into a science of it’s own founded by work based on Huxley’s three principles of biology by TINBERGEN which urged academics to apply more rigorous experimental techniques and turned a largely qualitative subject into the quantitative science that it is known by today. However this transition has not been easy and during this paper I will outline how the scientific community has approached the subject over the years. I will start by outlining the work done by TINBERGEN and then move onto how his ideas of what the subject was has shaped what it has become.

TINBERGEN described ethology as “the biological study of behaviour” in his paper “On Aims and Methods of Ethology” (1963). This was because at the time there was no consistent public view of what ethology was and even the academics involved differed in their opinion of what the subject entailed. He then broke down the field into two parts, the observable phenomenon (i.e. behaviour or movement), and more radically the method of study. Due to the complexity of the subject this was further broken down into different questions that should be addressed based on the previous work of HUXLEY. His work was on the “three aspects of biological fact”;

“Every biological fact can be considered under three distinct aspects. First, there is the mechanical-physiological aspect: what is the functional use of the organ or process, what is the biological meaning or value to the organism on question? And in third place, there is a historical aspect: what is the temporal history of the organ or process, what has been it’s evolutionary cause.”

Huxley’s work established a procedure or rather a general scientific method for approaching the biological study of an organism. TINBERGEN used these three aspects, causation, survival value and evolution and with the addition of ontogeny created a general scientific method for the study of animal behaviour. However as TINBERGEN admits it is the life’s work of Konrad Lorenz that made ethologists apply “biological thinking” to the field.

Konrad Lorenz was a pioneer in the field of ethology, working on the development of behaviour, such as imprinting in birds; he showed that animal behaviour could be studied in fundamentally the same way as any other biological phenomena. Believing that behaviour is part and parcel of the adaptive equipment of animals, it can be studied in the short term, it’s survival value calculated and it’s evolutionary aspects are comparable to the current methodology employed by biologists in other fields.

BAKER (1938) and MAYR (1961) also contributed to the groundwork of current ethology by grouping the methods of ethology into the proximate and the ultimate. BAKER made the distinction between the proximate, the “How?” questions to ask, such as “how did the animal perform this behaviour?” and the ultimate, the “Why?” questions, such as “why did this animal perform this behaviour, what is the adaptive significance of it?” MAYR related these questions to functional biology and evolutionary biology. Although the use of such easily misinterpreted descriptions, as we shall later, has probably done more harm than good.

TINBERGEN’s 1963 paper reviews LORENZ’s ideas about how a more analytical approach to ethology can be achieved and what his impression the current field encompassed with respect to the two parts, observation and methods, and the subsequent four aspects. He begins with looking how observation and description is carried out and how it can be improved in order to move the field away from the qualitative.

Observation

He stated that the roots of ethology began with naturalists and animal keepers pondering the question “Why do animals do what they do?” This was seen as a reaction against psychology at the time as although both concerned the behaviour of animals, psychology focussed on a few observable phenomena in a few species in captivity and claimed the results to be general. Ethologists did not agree and felt that psychologists had lost touch with the natural world and in order to understand the biology of an animal you must observe it in its natural surroundings. Since it was still a fledgling field there was a tendency for ethologists to write huge descriptive tomes of everything that a particular animal was seen to be doing. However this was all qualitative and what TINBERGEN did was to suggest how to move onto a more quantifiable method of description. Although this was not simple (every observation is subjective due to the observers preconceptions) he felt it important to stress the need to clarify standard criteria for selection.

Methods of study

However it was in the methods of studying ethology that TINBERGEN made the greatest advances. By sectioning them up he was able to tackle the problems concerned with each one individually.

1. Causation “How was the behaviour executed?”

LORENZ made three important statements earlier in his career regarding the aspect of studying causation that should be remembered:

A: Behaviour patterns are organs specially adapted to perform specific functions.

This allowed behaviours to be looked at objectively. Another difficulty was the tendency to see these functional organs as organs of mechanism ...

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Methods of study

However it was in the methods of studying ethology that TINBERGEN made the greatest advances. By sectioning them up he was able to tackle the problems concerned with each one individually.

1. Causation “How was the behaviour executed?”

LORENZ made three important statements earlier in his career regarding the aspect of studying causation that should be remembered:

A: Behaviour patterns are organs specially adapted to perform specific functions.

This allowed behaviours to be looked at objectively. Another difficulty was the tendency to see these functional organs as organs of mechanism for example nest building, although two different species of bird may do it their execution will be different. The repeatability of certain behaviours within a species suggests that some are species specific although they are not necessarily innate.

B: These organs are vastly more complex than their physiological counterparts.

TINBERGEN considered this of great importance as it highlighted the lack of communication between ethologists and physiologists at the time. It was stressed that this lack of communication between disciplines will do a great deal of harm to the field by creating boundaries where there were none, merely grey areas. His foresight was accurate as this did occur in the 1970’s. He thought that there was also an aversion to writing the tomes of descriptive text that had lead ethologists recently to oversimplify behaviours, which could be avoided if stricter analytical procedures were applied.

C: Initiation, co-ordination and cessation of behaviour patterns are controlled by the external world to a lesser extent than previously thought.

The field had moved on since the ideas that hormonal control was simply selective interaction with tissues and was entering into more complex ideas regarding feedback phenomena and growth related processes. The act of complex behaviour cannot be simply controlled by a single part of the central nervous system.

2. Survival Value “What is the adaptive significance of the behaviour?”, “Why did it happen?”

In the post Darwinian era a reaction against uncritical analysis of selection theory was initiated. Although this was a good scientific reaction it escalated to the point where speculation about survival value was taboo and people lost interest in the subject. However LORENZ never conformed to this fashion, believing that behaviour was an organ that the species had evolved as a means of survival.

TINBERGEN disregarded the statement that measurement of survival value was guesswork due to the confusion with natural selection (a previous action that can only be inferred). The survival values of current species are just as much open to experimentation as is the causation of behaviour and good studies have been performed (see MOSEBACH-PUKOWSKI 1937 on Vanessa caterpillars). Noticing species-specific behaviours is the first step, and this can be accomplished by spending a lot of time with the species in question. Also the writings of good naturalists are teeming with such hints, arguments and occasional demonstrations of the multitude of species-specific behaviour.

TINBERGEN outlines effective ways to develop a hypothesis test. The first is from LORENZ noting that animals in captivity display a number of behaviour patterns that seem to “misfire”. The behaviour patterns must be good for something and this will make the observer try to see the behaviour in it’s natural context. Another method is deduction of a hypothesis through comparison. Giving the example of the rocking of cryptic animals TINBERGEN states that if sufficiently different species display the same kind of behaviour then it can be hypothesised that there is convergent evolution and a selection pressure can be inferred relating the behaviour to a survival value.

However these hypothesis must be backed up by quantitative experimentation (the ultimate aim of TINBERGEN) will prove to be difficult as how is it possible to remove one behavioural mechanism whilst leaving the others intact. This approach relies on the use of dummies and to control their behaviour. Although some experiments are impossible to perform and so we must be satisfied by the fact that the advantages outweigh the disadvantages of the behaviour.

3. Ontogeny “How did the behaviour develop?”

TINBERGEN voiced the global agreement that in order to attain a complete understanding of behaviour requires an understanding of its ontogeny (development). Also that a central issue in behaviour development seems to be the question raised by the fact that so many behaviour patterns can be said at the same time innate and learned or partly innate or partly learned. Different components of complex behaviour have different origins but he was keen to stress that the desperate search for the origin of these components was futile. I happen to disagree as I think in order to understand the behavioural biology of an organism as a whole we must dissect it fully. However it is important that we do not get bogged down with our investigations and step back to see the wider picture.

4. Evolution “Where did the behaviour come from?”

TINBERGEN believed that evolutionary study had two major aims; the elucidation of the course evolution must have taken, and the unravelling of its dynamics. The first is best approached by comparing closely related species behaviours and looking for common descent. This method was encouraging as at the time taxonomic classifications based on behaviour were closely related to those based on structure. However I believe that one cannot believe that a face value due to the subjectiveness of the observer skewing the results. The evolution dynamics were split into two parts; the genetic control of species-specific behaviour, and the influence of selection on behaviour evolution. The genetic control is interesting as it opens up a huge field for discovery at the time where almost nothing was known and the effects of mutations on behaviour was just being investigated.

TINBERGEN noted that:

“For an assessment of what selection can be assumed to have contributed to the present sate of species it is important to realise that selection rewards or penalises isolated bits of animals by rewarding or penalising animals or breeding pairs as wholes.”

This relates to DARWINS's theories that natural selection enforces certain compromises on animals and TINBERGEN has linked this to LORENZ’s theory that behaviour mechanisms can be regarded as organs and therefore undergo the exact same compromises that structural features of an animal.

Experimentation for this question is difficult as you cannot ascertain detailed behaviour from the fossil record, and TINBERGEN reminded fellow ethologists that even the most perfect experiment would not give you direct proof of what occurred in the past.

In conclusion TINBERGEN’s paper served to give the study of ethology a more defined structure to which research could be based on and made more reliable and easier to compile into a complete view of the behavioural biology of an animal. However his paper was not without flaws and some of them I believe profoundly affected the course that ethology took.

After TINBERGEN’s Paper

Over the years, as the field of ethology itself evolved, discrepancies in the original plan laid out by TINBERGEN were becoming increasingly apparent and so naturally revisions were made. One of the main problems were the problems themselves, or to be more precise the terminology that was used to describe them.

HAILMAN (1973) condemned the use of survival value as it placed no emphasis on the cross generational inheritance of the behaviour, which is much more important than whether the individual survives or not. He suggested the use of “function” to describe the way that the fitness of the individual is enhanced by the behaviour. But the word function, like others is fraught with misconceptions. The modern day name is “adaptation”, this leaves no query as to what the related question is, i.e. what is the effect on fitness and survival of this adaptation to the animal.

The use of “causation” has been changed to “mechanism” as there are undertones of the history of the behaviour in causation when the question really centres on the process of the behaviour.

Ontogeny has been changed to “development” for better clarity, as has “evolution” been changed to phylogeny as it is more specific to the evolutionary history of the behaviour.

All this may seem pedantic but I would argue it does hold an important place, as TINBERGEN’s original questions were not sufficiently robust enough for modern ethologists. Due to the amount of data we now have and the experimental procedures open to us, it is vital we ask exactly the right kind of questions otherwise a lot of time will be wasted in retreading other peoples footsteps. TINBERGEN’s question were correct at the time of going to press, ethology was only just starting out as a field, but if the structure of ethology isn’t evolved then we may find ourselves unable to approach new areas of study or even worse get sidetracked down one line, not answering the other questions as they are seen to be outdated. This happened in the 1970’s with respect to the increase in interest in adaptation analysis. DAWKINS (1989) and DEWSBURY (1992) both produced papers urging the ethological community to regroup, assess the damage already done, and reassert what the common goal of the field.

During the 70’s there was a trend towards the emphasis of adaptation as being the major study of ethology. WILSON’s book in (1975) on “Sociobiology” spawned a new subset of ethology which quickly moved into becoming a discipline in it’s own right, Sociobiology. It as seen as fashionable at the time to be called one of these and so a lot of ethologists made the transition. This had many implications, although it may of seemed that all they were doing was renaming the question as before what occurred was a division of ethology into its component questions. Study of the mechanism of behaviour was deemed Neuroethology and phylogeny was shoved into Applied Ethology. The questions regarding the evolutionary aspect of behaviour were pretty much forgotten about, as they were deemed too hard to answer at the time.

Sociobiology was becoming more popular at the expense of the other questions, not the intent of TINBERGEN at all where he envisaged an equal distribution of effort between all the separate questions. Due to the advancements in experimental techniques at that time sociobiology produced reliable and larger amounts of data, the other questions were left on the shelf gathering dust. Sociobiology and Behavioural Ecology were seen as the be all and end all of ethology whereas, according to TINBERGEN, they were only part of the field of ethology. General consensus focused on the “ultimate” causes and saw the “proximate” causes as being unimportant.

Although the study of one particular question in more detail may not seem like a huge problem the point that both DAWKINS and DEWSBURY made was that it was at the detriment to the study of the other questions and therefore the field of ethology in general. DAWKINS put it as:

“Ethology may still be a four legged animal, but it is an animal that is hopping around on one big leg.”

DAWKINS saw the sectioning up of the science as dangerous due a point that TINBERGEN stressed in his work that of the lack of communication between disciplines. TINBERGEN noted that the ethologists and the physiologists of the time didn’t talk enough to each other and this lack of communication hindered the advancement of ethology as a whole. DAWKINS made the point that the very field of ethology had been split up into separate disciplines and now they were not communicating with each other. The fact that there was no central aim to ethology anymore, it is debatable that ethology really existed in those times, meant that the discipline were able to start formulating their own questions and moving research into areas that were not compatible with each other.

DAWKINS used the example of Neuroethology and showed the current incompatibility between disciplines. Neurobiologists could map entire nervous systems of simple animals but they had to refer to text 20-30 years old to relate their data to how the animal used this nervous system in behaviour. This because the neuroethologists worked on more “interesting” and complex animals and failed to ask the questions neurobiologists wanted answers for. She also wrote about how the neglect of certain questions forced the sectioning of the others, hence the creation of applied ethology.

DEWSBURY felt that TINBERGEN’s paper although important at the time failed to group the questions together into some for of hierarchy. TINBERGENS argument for this would have been that all questions deserved equal weight but I concur with DEWSBURY that TINBERGEN’s failure to properly “glue together” the different questions by demonstrating the overlap between them facilitated the breakdown of ethology into it’s separate disciplines later on. This wasn’t the original intention, quite the opposite in fact, but because TINBERGEN laid out exactly what types of questions should be asked research was funnelled into those areas and it as inevitable that if one question were to receive more attention the possibility of it separating and becoming a science of it’s own was inevitable.

Therefore DEWSBURY proposed a reformation of the current four questions believing that although they had a place, ethology was now a too dynamic subject to constrain to those questions anymore. He used current arguments at the time to emphasis the need to reform the structure of modern ethology. For example noting that GOULD & LEWONTIN (1979) emphasised that the 4 problems are non-inclusive because behavioural patterns can be induced environmentally without change in the genotype and they can be learned and transmitted culturally as well as genetically. Modern thinking had discovered areas that fell outside the original 4 problems. Although his reformation never caught on I believe it is worth a quick note as it went a long way to delineating the study of ethology by grouping together the different areas of study and making the links between them clear. His proposed idea is shown in figure 1:

Figure 1

I will only give a brief explanation as since this ideal never found footing in the ethological community there is little point elaborating in this paper. Genesis refers to the influence of past events (usually over a long time span) of the behaviour under study. Control is the short-term regulation, or causation of the behaviour, and Consequences are the results of engaging in behaviour to the organism itself other organisms and the environment, which can ultimately loop back and cause the genesis of new behaviours.

Because this reformation doesn’t specify questions, merely point out the different areas of study it is in no danger of sectionalising the science again as it is flexible enough to accommodate new headings when ethologists approach them. For these reasons I personally think that this is the best way of describing a discipline as there is no confusion surrounding the outline, unlike TINBERGENS questions, and it provides a framework for discoveries toe hung off.

Conclusion

Although some may see TINBERGEN’s paper as being seminal I believe that it also housed the seeds of it’s own demise. Whilst it provided important groundwork for the study of ethology it was not flexible enough to accommodate the subsequent advances in the field which lead to confusion among the meaning of the questions, debate over the terminology used to describe the questions and through it’s sectioning up for ease of understanding it’s components it contributed greatly to the creation of sub-sciences and the overemphasis imposed on some of them. The lack of communication is the major point here that with division comes segregation

However it seems that today ethology has come full circle and returned to the concept of the 4 questions, but with this time refined terminology. I believe that this is a foolhardy and temporary measure as ethology is simply not like any other science; it relies on the work from so many disciplines. To define the structure of the science as a series of questions inherently facilitates the division of the science. This cannot happen as ethology is such a broad subject that each member must always consider the common aim, otherwise segregation will occur and the lines of communication will once again break down and the cycle will repeat itself.