166 BIEB Lecture 3
Latest revision: 1/16/07, 3:54 PM
BIEB 166: ANIMAL BEHAVIOR & COMMUNICATION
LECTURE 3 READING: Classical Ethology Part II
I.
Umwelt
What would it like to hear with ears of a bat, sense electric currents like an electric eel, or
smell the world through the nose of a dog? An animal's senses shape its experience of the
world and thus play a critical role in the way that it behaves and interacts with its
environment. Indeed there are many potential stimuli that most animals cannot perceive. For
example, we cannot perceive cosmic rays or gamma radiation. One way to conceptualize
these stimuli is to use "stimulus sets". Stimulus sets form a hierarchy in which we can
categorize all environmental stimuli. First, the sensory physiology of the animal controls
what it can perceive and thus creates its perceptual world. Second, there is the set of all
effective stimuli that can elicit behavior. Third, there is the set of all key stimuli that will elicit
FAPs. Fourth there is the set of all key stimuli to which an animal responds in a given
motivational state. This last category is called the "Umwelt", German for "surrounding world."
Jakob von Uexkll applied the term "umwelt," to a specific ethological meaning. In this
context, an animal's "umwelt" is the subset of perceptible stimuli to which an animal
responds when in a given motivational state. In other words, there are several sets of stimuli
to which animals are sensitive, depending upon their motivational state.
For example, consider the water beetle Dytiscus. This predatory aquatic beetle has large
eyes and good vision. When searching for tadpoles to eat, it first uses only its sense of
odor. Showing a tadpole behind a sheet of glass to a beetle elicits no reaction. But if you
rub a cotton swab on the tadpoles skin and drop the swab into the water, the beetle is
immediately attracted to the swab and attacks it. Thus although the beetle can see the
tadpole behind the class, hunger causes it to focus on an umwelt of chemical stimuli.
The fritillary butterfly, Argynnis, provides another umwelt example. Like the honey bee,
these butterflies have good color vision that it uses when foraging for nectar from
flowers. It can easily be trained to pick blue or yellow cards from among a set of gray
shades of matching brightness. However, when a male butterfly pursues a flying female
during courtship he does not focus on color. The only cue that he responds to is the
wingbeat frequency of female's wings. Thus the male's motivational state (mating state)
determines the type of stimuli that he pays attention to.
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II.
Supernormal releasers
The Argynnis butterfly also illustrates another fascinating sensory phenomenon. You
can build a realistically-shaped butterfly dummy of any color, whose wings beat at the
right frequency, and it will attract males. However, you can also build a very unrealistic
dummy made of a cylinder with dark and pale stripes. You rotate the drum so that it
flickers at the right frequency. Eight beats/second is the normal frequency, and models
that flicker at this rate are very attractive to males. However, if one increases the rate
up to 75 beats/second, the model becomes more attractive to males than any real
female would be. This is a supernormal releaser effect. A supernormal releaser is
more effective than a natural key stimulus.
Another example of this is provided by the herring gull, which is attracted to the supernormally
large artificial egg, choosing to incubate it over her egg. Somehow the exaggerated version is
more stimulating to the Innate Releasing. Apparently, the neural representation of these key
stimuli in the Innate Releasing Mechanism is imprecisely designed, open-ended in the upper
range. This may lead to behavior that seems silly to us, but presumably in their evolutionary
history, gulls have never had to deal with giant eggs. Male butterflies have never seen a
female butterfly whose wings flickered at 75 beats/ sec.
Thus there has been no selection against such releasers.
Nestling cuckoos provide a third example. Cuckoos do not raise their own young. Instead,
females deposit their eggs in host nests. Thus cuckoos are brood parasites, parasitizing the
host, which raises the cuckoo chick as their own. Cuckoos chicks are adept at garnering
the most out of their foster parents. Nestling cuckoos Cuculus canorus exploit hosts with a
huge colorful beak gape pattern and begging calls that simulates the calls of an entire
brood of host chicks, thus inciting the hosts to provide more food and to neglect any of the
host chicks that the cuckoo chick has not already eliminated. Thus the supernormal stimuli
provided by the cuckoo are both visual and auditory.
III.
Interactive FAP sequences
Tinbergen pointed out that a given fixed action pattern can give rise to another fixed action
pattern. For example, in social behavior, the FAP of one animal can be the KS for another
animal. This can results in a cascade of alternating FAPs by two individuals. When two
animals are involved in a complex courtship ritual, this cascade of signals provides important
feedback about the identity of the participants, their reproductive state, and their quality as
mates. Such a cascade is called an interactive FAP sequence. The classic example of this
comes from Tinbergen's early work on the three spine stickleback. Other biologists have
often had trouble replicating some of Tinbergen's work, or have found that the story is much
more complicated than it initially appeared. No one doubts Tinbergen's integrity, but it is
clear that stickleback behavior can vary greatly depending on the precise experimental
context, and there is also a good deal of variation populations.
Keeping among that in mind, let's look at the story as it is usually told. Sticklebacks in some populations
spend most of the year in schools containing both sexes, but in the spring males leave their
schools and select a territory, a spot on the pond bottom suitable for building a nest. At the same
time, the normally greenish, pale-bellied males develop a striking color pattern, with a vivid red
belly and blue eyes. Within his territory, the male constructs a nest from bits of pondweed; here
we see a male trying to guide a female into his nest. Males at
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this time become very aggressive toward other males, chasing them away from their
territories. Tinbergen put two males in test tubes and moved them into the territory of
one of them. The territory owner immediately adopted a vertical, snout-down posture
with its spines erect. This is an aggressive display that releases an escape response in
the intruder. Chasing and possibly fighting if the two fish werent confined to test tubes
would follow this. When the tubes are moved into the intruder's territory, the roles are
reversed, and on the border each attacks and retreats about 50% of the time.
Tinbergen observed a curious thing. He found that all the males in his laboratory tank
went into the aggression display whenever a red delivery truck drove by the window. He
therefore suspected that the bright red belly of the male stickleback is a key stimulus for
other males. As he had when studying the gull pecking response, he turned to dummy
experiments to test his hypothesis. If a non-breeding fish or a non-red dummy is
introduced into a male's territory, the male rarely responds with an aggressive snoutdown display. The most unrealistically crude dummies, if they have a red belly, will
successfully elicit vertical displays. The vertical posture is a stimulus to other males as
well as a response: Red-bellied males elicit aggression in any orientation, but if plain
males are introduced into the territory confined in a tube can be positioned vertically or
horizontally, the vertical males release stronger aggression in the owner.
After the males establish territories, schools of females move into the area, and the males
swim toward them with a peculiar side-to-side darting motion called the "zig-zag dance".
How do males identify females? The females bellies are swollen with eggs. Tinbergen
offered territorial males both a swollen-belly dummy and one without the swollen belly; only
the swollen dummy released the zig-zag dance. He also offered a spherical, utterly nonfishlike dummy, which he regrettably referred to as the "sex bomb." This dummy served as a
supernormal stimulus, releasing wildly enthusiastic zigzagging in the males.
So far we've been talking about the male's responses; but what about the female's response?
Well, the male zig-zag dance is in turn a key stimulus for the female, who responds to it with a
vertical acceptance posture, the "head-up". He responds to the female's acceptance display by
(1) swimming to his nest, and she follows. (2) She enters, (3) he swims around to the back and
(4) he quivers his snout against her tail. This stimulates her to lay eggs, after
which she leaves and the male releases sperm. The male will go through this
process with sometimes more than 10 females, collecting immense numbers of
eggs before their care demands so much of his time that he has to spend all his
time with them, guarding them and fanning them to oxygenate them.
As with males, Tinbergen used a series of male dummies to determine what key stimuli
release the female's responses. Females ignored realistic dummies without red bellies,
but roughly half responded to red-bellied dummies of any shape. If he moved the palebellied dummies in imitation of the zigzag dance, they elicited a vertical response from
about half the females. Dummies that both zigzagged and had red bellies, whatever their
shape, released the vertical display in all females. Thus females require both color and
motion to release their fixed action pattern and proceed to mate.
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However, as these experiments and studies of many other animals indicate, the key stimuli
that elicit responses are very often highly schematic and stylized. As long as they have the
relevant key stimuli, unrealistic models are as effective as extremely realistic models.
IV.
Search images
In addition to the reproductive and escape, key stimuli can also be used to find food or other
resources. A search image is a key stimulus used by a predator searching for prey. Ticks
provide a good example of a search image. They respond to a very specific odor, butyric
acid, a principal component of mammalian sweat. The KS of butyric acid elicits the FAP of
releasing its grasp and dropping out of the foliage, and hopefully landing on a suitable host.
If you are interested in ticks, you can walk around in tick-infested woods with an open vial of
butyric acid, and they will drop on you by the dozens. After landing on a host, the tick then
shifts from a chemosensory to a thermosensory umwelt, orienting toward warmth in
searching for a spot to bite and begin to suck blood. Thus the umwelt changes, depending
upon the environmental stimuli that the tick receives. When the tick is hungry for a blood
meal and searching for a host, it orients towards smell of butyric acid. It has a specific
chemosensory umwelt. Once it locates and lands on a host, the tick is still hungry for a blood
meal, but now the stimuli that it receives are quite different. It senses the temperature of the
host. Now it is in the thermosensory umwelt. The environmental feedback that it receives
can affect its umwelt.