This lecture introduces you to some of the very elegant experimental methodologies developed by ethologists. Hopefully you will begin to appreciate that an animal's view the world in a very different way from ours - the dog lives in a 'smelly world', the owl lives in a nocturnal world of rustlings etc. - and how ethological techniques can be used to understand these worlds.
The lecture introduces the idea that behaviour as well as structure evolves.
The heart of the lecture is a discussion of how ethologists have used models to understand the significance of stimuli in an animal's world. You should avoid thinking of these techniques as only being applicable to the analysis of animal behaviour. You may find them useful in unravelling the complexities of human behaviour as well.
An ethological model of motivation is used to knit together some of the concepts introduced in the lecture. This model has some disturbing things to say about the inevitability of human aggression. By now you should be able to judge for yourselves the validity of the claims made by the model.
Studying the material on this page should enable you to:
Perception across species
| Flowers that appear to us to be a particular
colour may have distinct patterns (called honey guides)
when viewed in ultraviolet light.
Some insect eye's are sensitive to ultraviolet light and respond to the honey guides.
The important point about this example is that it shows us that animals may not necessarily perceive the world the way we do.
Just try to imagine how 'smelly' the world is from your dog's point of view or how the night is full of the rustlings of mice and other small prey to the barn owl. This may seem an obvious point, but it often appears to be missed.
For example, simplistic attempts to extrapolate from the behaviour of rats to human behaviour sometimes read as if they consider rats as "little human beings in white furry coats". On the contrary, they probably live in a world dominated by sensations transmitted to their brains through their vibrissae (whiskers on the side of the snout).
But it gets even more mysterious, we are probably not even aware of the sensory systems that control our own behaviour! Consider the case of human pheromones.
In 1971 McClintock reported that groups of women living together were more likely to have synchronized menstrual cycles than was expected by chance. Studies on women in university hostels show that within four months of living together their menstrual cycles tend to start at around the same time each month. And when women move in with men, their menstrual-cycle length shortens, so that they are fertile more often. McClintock & Stern tested if these effects involved pheromones. "The researchers collected body odour on cotton pads from women, and wiped them on the upper lips of recipient women. This was repeated daily over the next two menstrual cycles. The researchers found that the timing of the cycle was indeed altered in a systematic way. Odour from the follicular phase of the menstrual cycle accelerated the surge of luteinizing hormone, which precedes ovulation, and so shortened the menstrual cycle. Compounds from the same donors obtained later in the menstrual cycle, at ovulation, delayed the hormone surge and so lengthened the cycle."
You can read more about this fascinating research in this article in Nature (12 March 1998) : Lifelines: Communicating by body odours by Helen Phillips.
|Point to ponder
How would you investigate the effect(s) of female pheromones on human male behaviour?
What is the evolutionary advantage of pheromones?
by digger wasps
The digger wasp , Philanthus triangulum, builds a nest burrow in sand that contains developing larvae which she supplies with food. How does the wasp find her way back to the nest after returning from a hunting trip? Tinbergen concluded that she used visual cues around the nest on the basis of the following experiment:
- Whilst she was in the burrow Tinbergen placed a circle of pine cones around the entrance.
- When she emerged, the wasp reacted to the new situation by a wavering orientation flight (training conditions) before flying off.
- Returning with prey (testing condition), she flew to the circle of pine cones even though it had been moved during her absence.
The animation shows the wasp's flight behaviour during training and test conditions. You may need to watch it repeat a few times to understand what is going on.
Here is an interactive learning activity which allows you to explore the role of smell in the wasp's homing behaviour.
Fixed Action Patterns
Lorenz considered that every species has a repertoire of stereotyped behaviours called Fixed Action Patterns. Lorenz considered that they were
- innate and used the German word 'Erbkoordination' which translates literally as 'inherited co-ordination' to describe them.
- common to all members of the species (species-typical) and therefore they are as characteristic of the species as shared structural features
- once triggered by sign stimuli, fixed action patterns proceeded in the absence of the triggering stimulus. Lorenz noticed that egg retrieval by greylag geese proceeded even if he removed the egg after the behaviour had been triggered by an egg lying outside the nest. Here is a video of this behaviour.
The diagrams shows stereotyped courtship patterns in birds. We have already examined the courtship behaviour of sticklebacks, which is another example of a Fixed Action Pattern.
|Shaking display by great crested grebes: The pair face each, adopt an upright posture and shake their heads from side to side. You can watch a video of this behaviour (size:404K; opens in separate browser window)|
Fixed action patterns can be used to follow the evolution of behaviour because they vary between related species of animals. This analysis was one of the main interests of early ethologists.
Do humans exhibit Fixed Action Patterns? This question was addressed by Irenaeus Eibl-Eibesfeldt and Hans Hass who worked at the Max-Planck-Institute for Behavioural Physiology in Germany. They created a Film Archive of Human Ethology of unstaged and minimally disturbed social behaviour.
They filmed people across a wide range of cultures with a right-angle reflex lens camera i.e. the subjects did not realize that they were being filmed because the camera lens did not appear to be pointing at them! Eibl-Eibesfeldt has identified and recorded on film, several human Fixed Action Patterns or human 'universals' e.g. smiling and the "eyebrow-flash"
Eibl-Eibesfeldt took these pictures of a Himba woman from Namibia (SW-Africa). She shows a rapid brow raising (between the second and third still images) which coincides with raising her eyelids. Because all the cultures he examined showed this behaviour, Eibl-Eibesfeldt concluded that it was a human 'universal' or Fixed Action Pattern.
Further examples of Eibl-Eibesfeldt's films of human FAPs / 'universals' include:
- coyness behavior in different cultures
- emotions in a deaf blind child
- a cross-cultural overview on the occurrence of the eye-brow-flash.
Criticism of the term Fixed Action Pattern
Nowadays the term Fixed Action Pattern has been dropped from ethology and substituted by the phrases 'behaviour patterns' or 'behavioural acts' because:
- Behaviour is not as fixed as implied by the term Fixed Action Pattern. There are subtle variations between and within animals in, for example, the duration of individual components they vary around a mean value
- Fixed Action Patterns are not simply innate. They can be subtly modified by experience.
- Behaviour is modified as a result of the animal's environment - it is not always triggered in the presence of the external stimulus.
Sheepdog fetching sheep towards shepherd
|Consider the behaviour
of sheepdogs. Untrained sheepdogs have a tendency
to run around a group of sheep and herd them back towards
the shepherd. Possibly the dog regards the human as a participant in a
hunt for food. The shepherd builds on this natural herding tendency and
trains the dog to drive sheep in response to shouts and whistles.
Apparently it is difficult to train a sheepdog to drive sheep away from a human, and to leave one group of sheep to go and gather more. You can see these behaviours tested in the fetch and outrun sections of a sheepdog trial.
The outrun: Sheepdog herding sheep away from shepherd
Sign stimuli and releasers
In a previous lecture we have explored the courtship behaviour of the male three-spined stickleback.
In Spring male sticklebacks change colour, establish a territory and build a nest. They attack male sticklebacks that enter their territory, but court females and entice them to enter the nest to lay eggs.
Tinbergen (1951) used crude models of sticklebacks to investigate which features of male and female sticklebacks elicited attack and courtship behaviour from male sticklebacks.
This diagram shows Tinbergen's main findings:
- a model with a red belly was attacked
- a model with a swollen belly was courted
by male sticklebacks.
The term sign stimulus or releaser was used to describe simple features (e.g. red belly) of a complex stimulus (e.g. male stickleback) that bring about a particular fixed action pattern (e.g. head down attack behaviour in male sticklebacks).
The terms sign stimulus and releaser are sometimes used interchangeably. However ..
In this experiment Tinbergen investigated the stimulus responsible for releasing the gaping response in young thrushes.
He discovered that the birds would gape at a protuberance (head) on the side of a body model.
might think that the birds would gape at
the bigger head, but in fact Tinbergen found that the relative
size of the head was
more important than its absolute size. Presumably the birds preferred
the 'head' that was
the proper size for the model's 'body'.
||The natural world is
full of examples of releasers that have evolved to
allow communication between animals.
Some of the most colourful examples are the bright coloured plumage of male birds that help them attract mates.
In addition male birds often have behavioural displays that enhance their attractiveness to females. In contrast many female birds are relatively dowdy.
|This is seen in black
grouse where a group of males display in a 'lek' to inconspicuous
You can watch a video of the male black grouse display (size:776K; opens in separate browser window).
Evolution and behaviour
You will recall from the first lecture in this series that ethologists asked four questions about behaviour. How has it evolved and developed? What causes it, and what is its function? We are now going to focus on the first of these: How does behaviour evolve?
Ethologists have used the comparative method to attempt to reconstruct the history of a species. This involves comparing the behaviour of related species that exist today in order to understand their evolution.
This diagram shows the behaviour of four imaginary species (A,B,C and D) that are alive today. All four species share a common ancestor that lived millions of years ago which is represented by the red symbol on the diagram. The contemporary species exhibit behaviour that can be attributed to this common ancestor. Notice how the blue ancestor only contributes to the behaviour of three contemporary species (B,C & D) and so on.
This diagram makes the important point that the species we see in the world today have not evolved from each other. Thus species A is in one sense more primitive than species D, but species D has not evolved from species A. Instead we say that they share a common ancestor from millions of years ago. Thus the idea that humans have evolved from apes is a myth. Humans and apes share a common ancestor. This is one reason why it is interesting to study the behaviour of apes. This type of research may highlight similarities in the behaviour of the two species that can be attributed to our common evolutionary history - up to a point. The diagram also shows that each species is not simply the accumulation of ancestral behaviours. The foreground colour for each species is unique and different for each species. Thus contemporary species are much more than simply 'the sum of the parts of its ancestors'. Each contemporary species is unique, and the result of selection pressures during its evolution, and the evolution of its ancestors.
This is a very simplified diagram, it is possible for the same behaviour to evolve in species that do not share a common ancestor with the particular feature.
- Features that are similar because they have evolved from a common ancestor are said to be homologous. For example, the wings of birds, human arms, and pectoral fin in fish are all derived from a common ancestor
- In contrast, features that are similar because they have evolved in response to a common environmental pressure are said to be analogous. For example, birds and insect wings have evolved to support flight, not because birds and insects share a common ancestor with this feature.
Bower birds are a family of birds in which males attract mates by collecting brightly coloured objects which they display to females in 'avenues' or on 'maypoles'. There is an interesting relationship between the colourfulness of a male's plumage, the visual properties of the objects they collect, and the complexity of the structures they build to house these objects. Female bower birds are rather drab creatures. Some species of male bower bird are also relatively drab, but they make up for this by building elaborate structures decorated by brightly coloured objects.
to ponder: The next section contains details of the plumage
and bowers built by a number of species of bower birds that live in
Australia and New Guinea.
|The male Regent Bower Bird is brightly coloured but builds a relatively simple bower with a few leaves which contrast with the forest floor. These are arranged light side uppermost. This can be tested by turning a leaf over so that the darker side is uppermost. The bird returns this leaf to its original orientation.|
Bower Bird also constructs a simple bower consisting of
brightly coloured leaves. Although the male appears drab in this
picture he does have an eye-catching display for the female when she
has entered the bower.
Here is a video of the tooth billed bower bird display (size:398K; opens in separate browser window).
|This picture shows a female Satin Bower Bird inspecting an avenue of twigs a foot or so apart constructed by the male which has bright shiny blue feathers. The male arranges blue objects in front of this avenue.|
|This Western Bower Bird has constructed an avenue of twigs and arranged a collection of white objects in front of it.|
|Archbold's Bower Bird makes a simple clearing in which he displays his collection of exotic plumage, shells and beetle's wing cases.|
Bower Bird builds an extraordinarily elaborate bower
consisting of twigs arranged around the root of a tree fern.The twigs
have 'pendants' made of caterpillar droppings, the ring at the base is
constructed from compacted moss with rare fungi arranged around its top.
Here is a video of the male displaying his orange plumage to a female who has entered the runway at the base of the central 'May Pole' named after the ceremony in English villages which announces the beginning of summer
Supernormal stimuli is the phrase used to describe artificial stimuli that are more effective than the real thing in eliciting a behavioural response.
Herring gull chicks peck at a red spot on their parents's bill to induce their parents to regurgitate food. Chicks will also peck at a model consisting of a red spot against a yellow packground.
However it is possible to construct a model that is even more effective than a real head by using a red pencil with three white bars at the end. This is an example of a supernormal stimulus.
In this experiment the supernormal stimulus received about 25% more pecks from gull chicks than the natural head, a model of an adult head, or a model of the adult's bill (Tinbergen and Perdeck, 1950)
I wonder why animals respond to supernormal stimuli more vigorously than to a more realistic model. You might expect herring gulls to have evolved so that they more closely match the characteristics of the supernormal stimulus. But a long narrow bill might have compromised their ability to feed. So clearly there is a balance to be struck here between the feeding demands of the adult and young birds.
But the existence of supernormal stimuli shows that there is room for evolution to proceed. If this were not the case evolution would only occur in the face of changing environmental conditions.
Are we sensitive to supernormal stimuli? There is no clear cut evidence on this point but humans do seem to spend an extraordinary amount of time improving on their basic physical attractiveness. But because these devices show such cultural variation it is difficult to say they represent supernormal stimuli that work for every member of our species i.e. they do not have the universal appeal we would expect from a sign stimulus.
|Lorenz claimed that the
behaviour patterns of caring for young and the
which a person experiences when confronted with a human child are released
on an innate basis by a number of cues that characterize infants.
Specifically the following characteristics are involved:
animals - such as red squirrels and dormice - also have these
characteristics that make them particularly attractive to humans and
they often appear as 'loveable' characters in books for children or as
soft toys. For example, the 'Squirrel Nutkin' character in Beatrix
Potter's children's books.
|Contrast this to the characteristics of cold, haughty arrogance associated with birds of prey. For example, the use of the imperial eagle on top of standards carried by soldiers in ancient Rome.|
|Some of these babylike
features can be seen in these pictures of two members of the all-girl
pop group 'The Spice Girls', one member is known as 'Baby Spice'
Human ethologists have examined the relationship between facial babyness and sexual attraction. See Supplementary websites below
Egg retrieval by herring gulls
Herring gulls lay eggs in a shallow nest on the ground. The eggs are green or brown in colour and are covered in dark blotches. If an egg rolls out of the nest it is retrieved by the parent.
In an elegant series of experiments, Baerends & Kruijt investigated what properties of the egg signalled to the gull that it should be retrieved back into the nest. They removed two eggs from the nest and placed two dummies on the nest rim. The dummies were of various sizes, shapes and colours.
The investigators were interested in exploring the birds' retrieval preferences:
- Are bigger eggs more attractive than smaller eggs?
- What is the effect of egg colour on this behaviour?
Position preference and egg retrieval by gulls
It proved impossible to carry out a simple preference test because when two identical sized dummies were placed on the nest rim, the gull usually revealed a marked position preference, retrieving the dummy on the left first (or vice versa).
To overcome this problem, Baerends & Kruijt employed a very elegant titration technique in which position was titrated againt size. In anthropomorphic terms they said to the gull
"OK, we know you prefer the egg on your left / right hand side, but if we put this bigger egg on the right / left hand side will you retrieve it first?"
This diagram shows the titration method of determining the value of an egg dummy.
The large brown circle represents the nest with one egg in the nest bowl and two dummies on the rim.
The numbers 7,8,9,10,11,12 refer to the size of the dummies, r is the ratio of the sizes of the dummies on the nest rim. The dummy chosen on each trial is indicated in black.
is the model to be measured.
Row 1: Determination of the value of the gull's position preference. Starting from the left hand sise, the first test with two size 8 eggs, shows that the right-hand egg is preferred. This shows that the bird has a preference for eggs on the right hand side. The next test (to the right) shows that this preference remains when a smaller egg (size 7) is substituted on the right hand side. The sequence of tests shows that the value of the position preference lies between r=1.3 and r=1.5.
Row 2: Determination of the value of model X. The control tests show that the position preference remains unchanged- the bird continues to show a right hand side position preference. The experimental tests show that the value of X lies between egg sizes 8 and 10. (After Baerends and Kruijt, 1973)
|Point to ponder
Can you think of any other experimental investigation that could utilise the 'titration method'?
The influence of egg size and colour on retrieval
Several types of dummy eggs were used:
- brown unspeckled
- brown speckled (i.e. natural coloured)
- green unspeckled
- green speckled
|The simplified results
of a large number of titration tests are shown in this diagram.
The picture shows the influence of egg size and colour on retrieval
numbers 4 to 16 indicate the relative sizes of the dummy eggs used in
Note that the gulls prefer a green background colour to the normal speckled brown colour of gull eggs.
For example, a size 5 green egg is more attractive than a size 6 natural coloured egg. Because they also prefer eggs with speckles, this leads to the surprising observation that a size 5 green speckled egg is more attractive than a size 8 natural coloured egg.
The important finding is that the preference for larger eggs remains the same when other features like shape and colour are changed. This means that each feature (colour and speckling) adds a specific contribution that is independent of the contribution of the other features. In other words the features are additive in their effect on the gulls' behaviour. This finding is consistent with the Law of heterogeneous summation, which holds that the independent and heterogeneous features of a stimulus situation are additive in their effects on behaviour.
At first glance this experiment can be a bit difficult to understand. It may be helpful to think of a titration experiment in more human terms.
The picture represents a hypothetical situation in which car manufacturers are competing for customers against each other.
In the middle of the picture is a row of four cars which compete in the UK market for a share of the market for small hatchbacks. They are shown in an arbitrary order of preference. This order could represents for example their market share, or an individual's order of preference.
upper and lower sections of the picture
shows the hypothetical effects of altering the cost of two models.
In the example, if the cost of the Rover Metro was increased by £500 it would loose its lead on the preference scale against its nearest competitor - the Subaru Justy. In contrast if Volkwagen was to reduce the price of its Polo from £9,850 to £9,500 it would make ground on its nearest rival the Vauxhall Corsa.
your understanding of these concepts by examining the following
Assuming the gull does not have a position preference, which egg do you think a gull would choose from each of the choices shown in this picture?
Remember that gulls:
An interactive version of this test is available here
|Points to ponder
Lorenz' Hydraulic Model of motivation
|Flyfishing for trout may
be an example of presenting a sign stimulus to an
animal in order to elicit a Fixed Action Pattern.
The artificial flies used by anglers resemble the living insect in some important aspects -e.g. size, shape and colour.
But as every flyfisherman knows a particulat pattern of fly that works on one occassion may not catch a trout the next time it is presented. The effectiveness of the stimulus is affected by:
This example shows the importance of internal motivational factors in controlling behaviour.
Artificial Mayfly used by flyfisherman
Natural Mayfly eaten by trout
Konrad Lorenz developed a model that brings together the main ideas of classical ethology to explain animal motivation. It should be emphasized that this is a model, it does not pretend to be an accurate picture of structures that actually exist within the brain. Instead it is a way of visualizing how various hypothetical systems work together to organize an animal's response to its internal and external environment. It is called a hydraulic model because it views motivation as a liquid whose accumulation and discharge influences behaviour. consequently some people call it 'Lorenz's water closet'
Action specific energy (motivational energy) accumulates in a reservoir until released by an appropriate sign stimulus, represented by weights on a scale pan, or until the pressure on the valve causes an action pattern to occur spontaneously (vacuum activity).
The consummatory response or Fixed Action Pattern(s) released vary depending upon how much action specific energy is released from the valve.
I have prepared the following resources to explain Lorenz's model:
Although Lorenz's theory of motivation has been severly criticized, nevertheless it does suggest experiments and helps to explain some experimental results which we will now describe.
Interaction between internal and external stimulation
According to Lorenz's theory the type of Fixed Action Patttern exhibited by an animal is a function of
- the amount of accumulated action specific energy (internal motivational state) and
- the sign stimuli (external stimulation) to which the animal is exposed.
Baerends and his colleagues have provided an elegant demonstration of this principle. Male guppies exhibit several Fixed Action Patterns in their courtship behaviour:
- sigmoid posture - a high intensity behaviour corresponding to position 6 on the trough in Lorenz's model
- sigmoid intention - a medium intensity behaviour corresponding to position 3 on the trough in Lorenz's model
- posturing - a low intensity behaviour corresponding to position 1 on the trough in Lorenz's model
The external markings of a male guppy vary with its readiness to show courtship. In terms of Lorenz's model, the external markings are an indication of the level of action specific energy for courtship.
The sign stimulus value of the female increases with her size.
Baerends conducted experiments in which males with different external markings were exposed to females of various sizes. The results of these tests are shown below and indicate that
- for each pattern of male courtship behaviour, the size of the female needed to elicit the pattern was less the greater the readiness of the male to court.
The diagram shows the influence of the strength of external stimulation (measured by the size of the female) and the internal state (measured by the colour pattern of the male) in determining the courtship behaviour of male guppies.
Each curve represents the combination of external stimulus and internal state that produces the sigmoid courtship patterns of increasing intensity (After Baerends et al, 1955).
|Consider posturing behaviour.
Examine the curve for sigmoid behaviour
how internal state and external stimulation have been operationally
defined in this experiment
This is another experiment which at first glance is a bit perplexing, so lets put a human face on it. The picture below illustrates the main concept behind the Lorenz model and the relationship between external sign stimuli, accumulating action specific energy and behaviour. In the diagram:
person in this picture would eat
ice-cream even if it was presented shortly after a meal, but wouldn't
eat any of the other
foods. But if 10 hours had passed since their last meal they would eat
a beefburger if it
was the only food available!
in male cichlids
Can Hydraulic Theory explain these results obtained by Rasa (1969)?
This diagram shows the effects of three different living conditions on aggression in cichlid fish.
Lorenz's hydraulic theory of motivation
account for the increased aggression in isolated fish. One
interpretation is that in the
isolated male, aggressive action specific energy
increases which must find an
outlet and consequently the male becomes aggressive to the female he is
living with. If
this explanation can you explain why the total amount of
|Point to ponder
What are the implications of this research for understanding and controlling human violence?
You may find some of the material from the course Integrative Topics in Psychology: Aggression useful
Model of motivation
Deutsch's model addresses a fundamental weakness of Lorenz' Hydraulic mode. It includes a feedback link from the environment to the Analyser component which signals to the animal that its goal has been achieved. In turn the receptor system inhibits the Central link (shown in blue) and thereby the Motor link which is responsible for triggering behaviour is switched off.
The textbook by Slater gives a very good analysis of the strengths and weaknesses of Lorenz's model of motivation.
References and recommended reading:
does the wasp find its way back when it is out of sight of the nest?"
Recent work by Rudiger Voss and Jochen Zeil of the University of Tübingen, Germany, may provide an answer. They found that "Bees and wasps often use highly structured flight patterns to collect all the views of an object that they need to recognize it again. 'Learning' flights are made at any new food source or nest site. When leaving the site, the insect turns back to face it, and arcs from side to side keeping the nest or food site to one side, and prominent landmarks in the centre of its line of sight.
The insects seem to memorize a series of 'snapshots' of the scene, like taking a picture at the end of each arc. On approaching the site again, the insects tend to follow a flight path that takes in at least some of the same positions, where it can match the view to the picture it has remembered. "
More details on this work are available in this Nature piece: Lifelines: What a wasp sees by Helen Phillips
|Andrew Giger is a
neuroscientist working on bee vision. Part of his work involves
training bees to discriminate between two different visual patterns. He
wrote B-EYE as a tool to give him some idea what bees perceive.See the
world through the eyes of a honey bee
I strongly recommend you look through Philip Lehners's book "Handbook of Ethological Methods", 2nd Ed, Cambridge University Press, 1996, if you are interested in reading a comprehensive discussion of ethological methods. He covers the lot! - How to select a behaviour to study, how to describe behaviour, how to record it, and how to analyse your data.
is a nice example of contemporary research in what is now called
'behavioural ecology' - a discipline that has its roots in ethology.