Peter Kabai: Ethology lecture notes

What is ethology (and what it is not)?

Konrad Lorenz Konrad Lorenz (1960) defined Ethology as "the application of orthodox biological methods to the problems of behaviour". This definition brings all disciplines of biology focusing on behaviour in the realm of ethology from the genetic and neural control to the evolution of behaviour while clearly differentiates ethology from other branches of science interested in behaviour e.g. psychology or sociology.

Early ethologists focused on the function of behaviour, but they were interested in the mechanism, that is the genetic and neural control of behaviour as well. However, as methods to study genes or the neural system shaping natural behaviour were not available at that time such research did not lead to important discoveries. A later definition by Eisner and Wilson (1975) restricted the field of ethology to "...the study of whole patterns of animal behaviour under natural conditions, in ways that emphasize the functions and the evolutionary history of the patterns".

Nowadays many scientists in the field associate the term ethology with observational study of natural behaviour, and the term ethology is being replaced with behavioural biology, especially in the English speaking world. In this course ethology is meant to include all biological research on behaviour. Such a broad approach is corroborated by diversity of topics of the international conferences. For an example see program of the XIX IEC hold in Budapest, Hungary in 2005.

What is behaviour?

Behaviour in the everyday sense is "anything that an organism does involving action and response to stimulation" (Merriam-Webster), something we can see without special equipment. Non-living things, even mathematical formulas can exhibit behaviour "as the way they function or operate" (Merriam-Webster).

Ethologists have been trying to define the subject of their field in many ways but never reached a consensus. Levitis et al. (2009. free full paper) surveyed 174 ethologists and found a "surprisingly widespread disagreement as to what qualifies as behaviour". The authors suggested their own definition as "behaviour is the internally coordinated responses (actions or inactions) of whole living organisms (individuals or groups) to internal and/or external stimuli, excluding responses more easily understood as developmental changes". This paper got two citations in two years indicating that the behavioural biologist community was not shaken by the precise definition given by the authors. (See more on this at NYT)

Indeed, defining behaviour is not an easy task. As an ethologist I may be interested to study the movements of a tail shed by an escaping lizard (e.g. see Pafilis et al. 2008. pdf), even though a tail is less than the "whole living organism". In lack of precise definition we can accept that behaviour is whatever ethologists study. In the narrow sense ethologists study how living things operate, therefore behaviour is whatever can change in a short time scale and such changes are externally observable. In this narrow sense the growing process of antlers is not behaviour. The way a red deer stag uses its antlers is behaviour. In the broad sense the growing of antlers and the final product itself are considered "behaviour" because the size and shape of the antlers are part of the same evolutionary strategy to win the battle for reproductive success. Therefore any individual characteristic can be studied by ethologists and is considered as behaviour.

The lack of a good definition of behaviour does not hinder ethology as much as it does other branches of science. For one example Furr (2009 free full paper) as a psychologist defines behaviour as "verbal utterances or movements that are potentially available to careful observers using normal sensory processes" - very similar to our "narrow sense" definition and receives a number of diverse comments (abstracts). For another example see the enlightening and funny paper on the application of behaviour concept on robots and how ethologists interpreted robotic behaviour (Vaughan at al. unpublished).

Purpose, introspection and anthropomorphism

Animals do various things which benefit them; they eat, hide from predators, and seek mates. A given series of actions seem to have a goal, because when achieved the animal would do other things. It is tempting to assume that the animal has a purpose and even some scholars would use purpose as a synonym of function: "The ethological method of research is mainly used to establish the function (purpose) of an animal’s behaviour". Purpose, an intended or desired result, even when exists, however, is not necessarily the function of the behaviour. You reach for an apple with the purpose of enjoying the flavour. Hunger for fruits, however, was not designed to give you pleasure. It is the other way around, the good feeling when eating the apple evolved to make you get nutrients and vitamins. Humans - unlike other animals - can talk about the purpose of their actions, however, the self-reported purpose is often different from the biological function of the given behaviour. In many cases we do not know the function of our behaviour, and sometimes we do not report our assumed purpose ("Language was given to men so that they could conceal their thought" - Talleyrand). I would add that thought was given to men so that they could conceal their true biological motivation. This is one of the reasons why self-reported behaviour or purpose are considered unreliable even in psychology (Furr 2009 free full paper).

Without rigorous scientific methods philosophers and early psychologists had to rely on the study of their own thoughts, desires and purposes. This method called introspection was used to understand human nature and by some scientists also to infer the nature of animal behaviour. Looking at animals as at somewhat limited human beings is anthropomorphism.

The following is an excerpt from Animal Intelligence by George Romanes published in 1884 (free full book)

"The excrement of the young of many birds who build their nests without any pretensions to concealment, such as the swallow, crow, &c., may at all times be observed about or under the nest ; while that of some of those birds whose nests are more industriously concealed is conveyed away in the mouths of the parent birds, who generally drop it at a distance of twenty or thirty yards from the nest. Were it not for this precaution, the excrement itself, from its accumulation, and commonly from its very colour, would point out the place where the young were concealed. When the young birds are ready to fly, or nearly so, the old birds do not consider it any longer necessary to remove the excrement."

Here Romanes suggests a function of the behaviour and by analogy to human thinking speculates that birds are able to consider predation risk and interprets the removal of the excrement as a result of conscious purpose. To understand the mind of birds by analogy of human cognition is anthropomorphism. Such analogies were treated by Romanes as evidence as he describes his method in the Introduction: "Starting from what I know subjectively of the operations of my own individual mind, and the activities which in my own organism they prompt, I proceed by analogy to infer from the observable activities of other organisms what are the mental operations that underlie them."

If you watch this clip bellow it should be clear that young chicks do not "consider" to present faecal sacks but rather do it in a stereotypyc manner, at a very young age without being able to observe others doing so, which alltogether suggests that this behaviour is not learned.

Carolina Wren parent removes a faecal sack kindly presented by the chick

We can also assume that the response of the mother to the sack is unlearned too. Still, the question remains: carrying the sack to a distance from the nest can be a result of some "consideration". Until we find out the answere we can apply Morgan"s canon: let us assume carrying the sack is also an innate response.

The anecdotal approach of George Romanes was sharply criticised by Lloyd Morgan who suggested that "In no case is an animal activity to be interpreted in terms of higher psychological processes, if it can be fairly interpreted in terms of processes which stand lower in the scale of psychological evolution and development". This statement coined as "Morgan's Canon" was very important in the development of Comparative Psychology (see later)

The function of behaviour

Romanes postulated that the function of removing the excrement from the nest is to avoid the attention of predators. It may be so, but that behaviour may have a different or even multiple functions. In this case it is conceivable to assume that a nest kept dry does not attract insects as much as a wet nest, there would be less parasites, fungi and bacteria, the chicks can remain dry which helps their thermoregulation, their feathers remain clean so fledging would be easier, the accumulation of large amount of faeces in a small space would be a physical barrier and/or decomposition of faeces would reduce oxygen supply, just to mention a few possible functions.

When speculating about possible functions of a behaviour pattern we list all the possible consequences of that behaviour. The real function is a consequence affecting the fitness of the individual. During a field research on the function of faecal sack removal one consequence will be notes accumulating on the sheet of the observer. Although observation of nests can affect the fitness of the bird (e.g. Livezey 1980 first page), however, we do not consider this as function, because an observational study is not a „natural” situation. In other words, birds did not evolve to remove faecal sacks to attract the attention of ethologists.

The function(s) of the behaviour - tu put it simply - is such consequense(s) of that action which have an effect of fitness.

Can any behaviour have negative consequences on fitness?

The short answer is no, any behaviour pattern is assumed to have a positive effect on the individual. Theory suggests that detrimental behaviour patterns are selected against in evolution and would eventually vanish. In real life, however, when considering possible functions of a given behaviour we should be very careful.

Artifial environment. Domestic animals in their artificial environment or wild animals in captivity cannot always perform their normal, adaptive behaviour. Does the monotonous spacing of tigers in the zoo, or air gulping by horses benefit the individuals? Are such stereotypies are part of beneficial coping mechanisms helping the animals to survive in their restricted environments, or are they detrimental for the individuals?

Ecological traps. Horseflies find water and host animals by polarised light reflected from their surface (Horváth et al. 2008 abstract). Manmade structures from gravestone through automobiles to the windows of skyscrapers reflect polarised light and attract horseflies to their misfortune. Such ecological traps are abundant, and lower the fitness of animals performing their normal behaviour.

Evolutionary arms race. The same behaviour can be beneficial in one, and detrimental in an other situation. Some fish will swimm to the surface if insects drop in the water - and eat them. That is adaptive. However, some herons catch live baits and drop them into the water to catch the approaching fish (first page of article or Higuchi, 1986 full paper).

Altruistic behaviour. Altruism, helping others with a cost for the helper, is not advantageous for the individual. How altruistic behaviour can still be maintained by selection we will discuss later. Here the point is that the consequences of some behaviour can be harmful for the actor.

How to study function of behaviour?

Function of any behaviour is the consequence of the action affecting the fitness of the actor. Based on observation, literature, comparisons with other species, and common sense we list all the possible consequences. Returning to the possible function(s) of faecal sack removal our list would look like this:

Removing faecal sacks may result in:

1) avoidance of the attention of predators

number of predatory events diminish

2) dry nest

less fungi and bacteria -> healthier chicks
dry feathers -> less accidents during first flight
more space for chicks -> ?
more oxygen -> may be important in cavity nests?

These are hypotheses about the function(s). To test the hypothesis we need to see the effect of the action and compare the effect with situations when the action is absent or occurs in a different form. This could be done by experimentation or by observation. For example as a preliminary experiment we can put as many sacks into a few nests as removed by the parents and see whether the parents would remove those additional sacks. They probably would not touch them, but if they do we could simply squeeze the sacks so the parents would not be able to grasp them. If that works, we should assign nests into 3 groups. One would receive the treatment, the second would receive a sham treatment meaning they will be exposed to all the manipulation as the experimental group without actually receiving sacks. The third group will serve as an additional control and will be left undisturbed so that would control for the effect of the manipulations. This simple experiment would require a huge amount of logistics and labour. Where do we get faecal sacks? Perhaps we could obtain the material from handfed chicks. If it is not feasible we could substitute the real sacks with some other material. Hand rearing chicks for experimentation is an ethically questionable, whereas substituting the real material may result in distorted results.

Most birds not only remove but also carry away or eat the sacks. If removal surves cleanliness exclusively, why would birds pay the cost of carrying the sacks? To answere that we could test whether faeces around or under the nests would attract predators. Petit et al. (1989 pdf) did such an experiment. They put out quail eggs in a forest and positioned 70 g of fresh chicken faeces at different distances of the eggs. Eggs very close - 10 cm - to the faecal pile were heavily predated while survival of eggs further away was much better.

Another approach is observation. For example one could compare the fitness of parents of different species with and without removal of faecal sacks. As species may be different in many other characteristics (e.g. one is more vulnerable to predation) ideally such species should be closely related and have similar lifestyles. As faecal sack removal is a complex behaviour involving cooperation between chicks and parents it is highly unlikely that such behaviour pattern was invented many times independently but rather inherited from ancestral species. This is why closely related species would probably either show or not that behaviour.
Observing the behaviour in one species under different circumstances seems to be more feasible. This was actually done e.g. by Weatherhead (1984 full pdf) in Tree Swallows (Tachycineta bicolor). He observed 10 nest boxes over land and 13 over water body. He reasoned that if faecal sack transportation is an antipredatory measure, birds nesting over land should carry the sacks longer distances than swallows nesting over the water, because sacks disappeare in the water. (Figure: male swallow carries a sack, click for large size.)

He found that carrying the sacs imposes cost for the parents and indeed, birds nesting over water dropped the sacks closer to the nest than birds over land. The results suggest that faecal sack transportation is an antipredatory measure. Would the hypothesis of antipredatory tactic rejected if no differences were found between land and water nesting birds? Probably not, because the distance a bird carries the sacks could be genetically programmed, independently of the habitat.

Such findings therefore rise exciting questions. The difference in the behaviour between land and water nesting birds can be explained in many ways. Is this an automatic, unlearned response, e.g. I see water I do not carry it far, I see ground I carry it further away? Or was Romanes right when speculating that birds do consider the effects of faeces in or around the nest? We do not know the answere - one plausible hypothesis could be that the urge to remove and carry the faecal sack in not learned - modification of that behaviour might be influenced by experience. Although Morgan's Canon played an important role in the development of psychology, nowadays ethologists tend to interprete behaviour "in terms of higher psychological processes", because assuming cognition in many cases seems more plausible than blame "instinct" for every single behaviour element.

Assuming that faecal sack removal serves cleanliness and transportation is an antipredatory measure may resolve the debate in the literature. But even this very simple behaviour raises still a plethora of questions. Many birds not only remove faecal sacks, but remove any object (twigs, leaves etc.) which do not resemble their own eggs. Could faecal sack removal have emerged as a side effect of general sanitation behaviour? Probably not, at least not in those species where parents actively stimulate the chicks to defecate. Such behaviour, moreover the interaction between parent and offspring is too specific to be a non-functional side effect. And then what is the function of sanitation? Simply to keep the nest cleen? Probably more than that. Moskat et al. (2003. pdf) suggested that birds reject all non-egg shaped object as a general cleaning mechanism, however recognition of their own eggs allows parents to reject parasitic eggs. Therefore nest cleaning can have many different functions.

Summary:

Konrad Lorenz (1960) defined Ethology as "the application of orthodox biological methods to the problems of behaviour".
There is no good definition of behaviour. In the narrow sense behaviour is movement or the lack of it and can be observed from the outside. In the broad sense any individual trait can be considered behaviour.

The function of a given behaviour is the consequnce of such actions. An action can have more than one consequnces, therefore any action can have more than one function. We should, however, be careful what we considere an action. There is some debate in the literature about the possible function of faecal sack removal whether it is sanitation or antipredatory measure. The same behaviour have both consequences, proposed functions are not mutually exclusive. Moreover, in this case removal and transportation should be considered as two separate actions with different possible consequences.

Ethologists avoid anthropomorfic explanations and do not assume that the animal performing a behaviour has a purpuse. Lloyd Morgan suggested that "In no case is an animal activity to be interpreted in terms of higher psychological processes, if it can be fairly interpreted in terms of processes which stand lower in the scale of psychological evolution and development". In recent years more and more cases have been described which can not be explained without the assumption pf high psychological processes, cognition in many non-human animal species.