Introduction to the study and definition of animal behaviour

1.4 Tinbergen’s four questions

Photograph of the greater sage grouse displaying on its lek. The bird has dark brown and white plumage and it’s feathers are erect.

The Greater sage grouse (Centrocercus urophasianus) from North America displaying on its lek

Work found at Licensed by Dan Dzurisin under the Creative Commons Attribution-NonCommercial-NoDerivs 2.0 Generic (CC BY-NC-ND 2.0) licence

In 1963 Niko Tinbergen published a seminal paper entitled ‘On the aims and methods of ethology’, which laid the foundation for how to conduct research in the fledging field of animal behaviour. The lasting contribution of the paper is that in it Tinbergen formulated four different, albeit somewhat interlinked, approaches to the study of animal behaviour, or four different types of questions we can ask about an observed behaviour.

The four questions are:

  1. Function (or adaption): Why is the animal performing the behaviour? In which way does the behaviour increase the animal’s fitness (i.e. its survival and reproduction)? Examples are plentiful and include, among many others, nurturing of young to increase their chance of survival, migration to warmer (and more food rich) habitats, escaping or avoiding attention from predators etc.
  2. Evolution (or phylogeny): How did the behaviour evolve? How has natural selection modified the behaviour over evolutionary time? This is typically addressed by the comparative approach, where the behaviour in question is compared among closely related species. Examples include how flight in birds may have evolved from gliding in dinosaurs or how the vertebrate and cephalopod eyes have evolved by convergent evolution, with the former having a blind spot, while the latter does not.
  3. Causation (or mechanism): What causes the behaviour to be performed? Which stimuli elicit or what physiological mechanisms cause the behaviour? Examples include the role of pheromones and hormones, such as increasing testosterone levels (caused by increasing day length) causing male display behaviour in many species of birds, moving shadows causing ragworms to withdraw into their burrows or contrast on beaks causing herring gull chicks to peck.
  4. Development (or ontogeny): How has the behaviour developed during the lifetime of the individual? In what way has it been influenced by experience and learning? Examples include how courtship behaviour improves with age in many birds and how predators learn to avoid toxic or dangerous prey with experience.

The four types of questions operate at two different levels. Questions 1 and 2 give ultimate or evolutionary explanations. These are answers that take a longer perspective and try to explain why the behaviour has evolved. On the other hand, questions 3 and 4 give proximate explanations. These are answers that look into the immediate mechanical reasons for why a behaviour is expressed. To obtain a full understanding of the costs, benefits and constraints that have shaped a given behaviour both ultimate and proximate answers must be obtained.

Some scientific experiments are designed to address only a single question, although many simultaneously address different questions. In our Manning and Dawkins (2012) textbook we find two different examples of how to use Tinbergen’s questions in analysing behaviour.

The first example looks at escape behaviours in cockroaches. When toads attempt to capture cockroaches by rapidly extending their tongues, cockroaches have evolved an escape behaviour where they very rapidly turn away from the toad and run away just before the tongue strikes. If we look at this behaviour with question 1 and ask what the survival value of the escape behaviour is, then it is obvious that this behaviour decreases the predation success of the toad and increases the chance that the cockroach survives an encounter. With question 2 we would ask how this behaviour has evolved by investigating different closely related species and see how their escape behaviours differ. By looking at different species of toads we could potentially also examine if the rapid turning and escape and the rapid tongue extension in these toads have co-evolved via an arms race between the toad and the cockroach. With question 3 we would ask how the cockroach senses the approaching tongue, which it does via special wind-sensitive hairs on its abdomen that can pick up the small puff of air created by the striking tongue and/or how this sensory information travels from the hairs to the muscles and causes the cockroach to rapidly turn and run away. Finally, with question 4, we can ask how this behaviour has developed. There is probably no learning involved since cockroaches that do not perform the escape behaviour successfully will not have the chance to learn from their mistake. Instead we can see how the escape behaviour develops throughout the maturation of the cockroach in connection with the development and growth of the number of hairs as the juvenile cockroach grows.

The second example looks at courtship displays in male sage grouses that gather at common display grounds, so-called leks, to perform the courtship struts. You can see an example of the sage grouse strut displays in the video below.

These behaviours are more complex than the simple escape behaviour in cockroaches and thus are not as easy to analyse in detail in terms of Tinbergen’s questions. Nonetheless, the question of function is relatively straightforward, since the females choose which males to mate with depending on the attractiveness of their courtship struts, so it increases the chances of mating and thus the fitness of the displaying male. The evolution question can be addressed by looking at how it has evolved from the simpler feather erection behaviour of related game birds. The causation question is much more difficult to address as we do not know the sensory and neural networks of these vastly more complex animals in the same detail as in cockroaches. However, at a higher level the behaviour is caused by the rise in testosterone in males, presumably linked to increasing day lengths. Similarly with the development question we can at a high level observe that younger males are far less successful in mating than older males, so some element of learning or maturation of the individual might be involved.

Individual activity: Tinbergen’s four questions

Think about a characteristic behaviour of two of your favourite animals. Then analyse the two behaviours choosing a different one of Tinbergen’s questions for each. First try to formulate the question and then do some internet research or hypothesise yourself to attempt to answer your question.

If you have come up with a good example or have any thoughts on this activity that you want to share with the rest of the class please feel free to post them in the Introduction forum.