Signalling and Reception
Secondary article
Article Contents
Leena Lindström, University of Jyväskylä, Jyväskylä, Finland
Janne S Kotiaho, University of Jyväskylä, Jyväskylä, Finland
. Introduction
. What is Communication?
Communication, a widespread natural phenomenon, occurs in both animals and plants.
Signals are evolved traits that transfer information from one individual (the signaller) to
another (the receiver); they can occur in any sensory modality.
Introduction
Communication is a widespread phenomenon in the
natural world, occurring not only in animals, but also in
plants. Signals are traits that have evolved specifically to
transfer information from one individual (the signaller) to
another (the signal receiver). They can occur in any sensory
modality, and some signals are even sent in several sensory
channels simultaneously. Signals have evolved to provide
useful information for receivers; a signaller provides this
information in an attempt to manipulate a receiver’s
behaviour to its own advantage. This conflict of interest
between signaller and receiver means that to be mutually
beneficial signals need to be honest, although under certain
circumstances, deceptive signals can evolve. The sensory
and psychological capabilities of signal receivers have also
influenced signal design, and the signals that we see today
are the product of selective pressures on both signal
content and how efficiently that information can be
transferred.
What is Communication?
Communication is the process whereby individuals send
and receive information about each other and their
surroundings. Communication is achieved through the
use of signals, traits that have specially evolved to transfer
information between one individual (the signaller) to
another (the signal receiver). Because signals have evolved
to transmit information, this distinguishes communication
from simple information acquisition. Psychologists often
use the term ‘signal’ to describe any stimulus in an animal’s
environment that might alter its behaviour. For example, a
tone might be a cue from which an animal learns to predict
the arrival of food and move towards a food dispenser, but
the sound is not a signal in this evolutionary sense as it is an
arbitrary cue designed by the experimenter. In addition to
communication between individuals, communication can
occur at other levels of cellular organization within
individuals, for example in cell to cell signalling. However,
here we focus only on those signals that are transmitted
between individual animals and plants. These can be
characterized by the signals being produced by a signaller,
. Honesty of Signals
. Signal Design and Receiver Psychology
. Signalling in Plants
transmitted through a surrounding environment, and
received by a receiver.
Signals can be either directed at conspecifics or at
members of other species. Intraspecific signals (i.e. those
occurring between individuals in the same species) can be
used to attract a mate, to deter rivals, to maintain social
grouping, or to warn kin of approaching danger. Signals
aimed at individuals of another species are often antipredator signals, for example, alarm calls, warning signals
and mimicry. Signals produced by plants are often aimed at
animal receivers; for example, flowers attract insects or
birds to pollinate them, although, as we shall see, there is
some evidence of communication between plants. However, first we will consider animal communication in more
detail.
How do animals communicate?
Animals have evolved an incredibly diverse array of traits
that they use for communication. Based on the sensory
capabilities of the signal receivers, signals can be considered to fall into three main categories: acoustic or
vibrational signals; olfactory or chemical signals; and
visual signals. In addition, electric signals are found in
some fish species that emit pulses from discrete electric
organs derived from modified muscle (Andersson, 1994).
Acoustic signals, as well as all other vibrational signals,
are mechanical stimuli that are transmitted through a
medium such as air, water or a variety of solid materials.
Depending on the medium in which the signal is sent, these
signals may be used for very short range communication
(e.g. plant stem vibrations produced by tropical wandering
spiders), medium range communication (e.g. airborne bird
song) and very long range communication (e.g. underwater
sounds and songs of whales).
Olfactory and other chemical signals are transmitted
through a medium by diffusion, which can be a slow
process if the viscosity of the medium is very high.
Olfactory signalling is commonly used by mammals, where
it plays a potent role in their social organization. Olfactory
communication is also widespread among insects: many
insects produce pheromones, a class of species-specific
chemical compounds or molecules that are produced to
communicate between members of the same species. In
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Signalling and Reception
addition, the use of scents or pheromones is not
uncommon even among birds, fish, amphibians and
reptiles. As with vibrational signals, olfactory signals can
be very short range, localized signals (e.g. urine marking of
many mammals) or can travel considerable distances (e.g.
moth pheromones).
In addition to sounds and odours, animals produce a
variety of visual signals. These traits are usually extremely
striking (e.g. the bright plumage coloration of many birds),
and often take conspicuous shapes and forms (e.g. the
eyespots and enlarged fins of some fish). In addition to
these morphological traits, some visual displays make use
of foreign artefacts and construction. For example,
tropical bower birds, such as the Satin bower bird
(Ptinolorhynchus violaceus), adorn their bowers with
colourful objects that attract females. Male satin bower
birds collect blue objects, ranging from flowers and bottle
caps to colourful glass, with which to decorate their
bowers. Movement is often used in visual displays, perhaps
to increase the detectability of morphological traits, as
these can only be received over relatively short distances.
This combination of movement with visual signals may be
regarded as a behavioural display, which often incorporates signals from other sensory modalities.
warn relatives of the presence of a predator. Interspecific
signals are perhaps less common, with signals that are
aimed at predators being the most well-studied.
Sexual signalling
The purpose of sexual signals is either to attract mates of
the opposite sex or to deter rivals of the same sex.
Ornaments are morphological traits that are used for mate
attraction and include the plumage and feather ornaments
of many birds, the colour markings of some lizards and
fish, and the leg tufts of certain species of spiders
(Andersson, 1994). Traits produced in other sensory
modalities can also attract mates: bird song and the calls
of crickets and frogs are examples of acoustic signals that
animals use, and olfactory signals are also common,
especially in insects. Other morphological traits and signals
evolve in response to competition between members of one
sex for access to mates in the other. These are used in
contests between individuals where weaponry and threat
signals are produced to deter rivals. Perhaps the most
striking examples of these are traits that are used as
weapons, such as the antlers of many ungulates and the
horns of some beetle species.
Social signalling
Multicomponent signalling
Many animals use complex signals that combine multiple
components. Multicomponent signals may have evolved
because they allow more effective information transfer, or
convey more information than single component signals.
These signals may be potentially more reliable, or more
difficult to ‘eavesdrop’ (see below). Multicomponent
signals can be either unimodal, i.e. they are perceived in
only a single sensory modality by the receiver, or they can
be multimodal and produced in more than one sensory
modality. For example, ladybirds (Adelia bipunctata) are
aposematic, in that they taste unpleasant to birds and they
signal this unpleasantness to birds using conspicuous
colouring but also by releasing a strong pyrazine odour
when attacked. Birds learn to associate these multiple
signals with unpalatability, and association is most
effective when both the colour and the odour are present
(Marples et al., 1994). Many sexual signals also have
multiple components, and signallers often incorporate
movement in a vivid behavioural display.
When do animals use signals?
Animals use signals in situations where they need to convey
information about themselves or their environment to
other animals. Signals are used in encounters between
individuals of the same species (conspecifics), but also in
interspecific interactions. Signals aimed at conspecifics
occur in a variety of social situations: for example, to
attract a mate, to defend a territory against a rival, or to
2
Social signals are used by conspecifics living in tight
groups. They can reveal the dominance and hierarchical
status of a particular individual within the group. Social
signals can also be cooperative when animals transfer
information that benefits both signaller and receiver; for
example, small passerine birds use alarm calls to inform
individuals within the same flock of an approaching
predator. Alarm calls benefit receivers as it provides them
with an opportunity to flee, but also protects the signaller
as it is less likely to be attacked in the flock than if it were to
flee on its own.
Warning signalling
Not all communication occurs between conspecifics;
signals can also be directed at receivers in other species,
such as predators. Usually the function of signals that are
directed towards predators is to escape predation. Warning signals, or aposematic signals, inform the predator that
there is a cost of attacking the signaller. Usually this cost is
that the prey is unprofitable in some way; for example, the
prey may contain chemicals that are unpalatable or are
emetic. Some animals with warning colours, such as the
yellow, red and black coral snakes or the redback spiders
(Latrodectus spp.), are deadly poisonous, and it is therefore
in a predator’s interest to avoid these species. The most
common and the best-studied warning signals are colour
patterns. A classic example of warning coloration is the
black and yellow pattern of monarch butterfly larvae, and
their black and orange coloration as adult butterflies. In
this particular species of butterfly, the coloration functions
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Signalling and Reception
to warn predators that they contain cardiac glycosides.
These chemicals are emetic for most predators, and the
recovery time after eating an adult butterfly may be up to a
half an hour.
Many aposematic species also produce multicomponent
warning signals (Rowe, 1999). For a long time, the different
components of these multicomponent signals, such as
odours, colours and behaviour, were thought to be directed
at different groups of predators; for example, visual signals
were thought to be effective against birds, while odours
warned nocturnally hunting mammals. Recent studies of
multicomponent signalling have, however, revealed that in
fact more than one signal may be directed at a single
predator (Marples et al., 1994). Thus, by having more that
one warning signal, prey can increase their chance of
survival against a particular predator (Marples et al., 1994;
Rowe and Guilford, 1996).
Honesty of Signals
A fundamental component of signalling systems where
there is a conflict of interest between the signaller and the
receiver is the maintenance of honesty in the signal. The
question is, what prevents signallers from cheating or
giving misleading information in their signals? This
question is particularly pertinent because theoretically an
individual can benefit from giving false information (see
discussion on deception and mimicry below). Signal
honesty was first appreciated through the idea of the
‘handicap principle’ (Zahavi, 1975; Johnstone, 1995). The
handicap principle was introduced in the context of sexual
selection and mate choice, but it is also applicable to many
other signalling systems: for example, signals from prey to
predators, from offspring to parents, and between opponents in agonistic contests. The handicap principle
proposes that signals are used by an intended receiver
because they convey honest information about the
signaller; however, signal honesty can only be maintained
if two conditions are fulfilled. First, signals must be costly
to produce or maintain for the signaller; and, second, the
cost must be dependent on the condition of the signaller,
such that signallers in good condition can withstand the
cost of signalling at a given level better than a signaller in
poor condition (Johnstone, 1995). The differential costs
between high-quality and poor-quality individuals is vital
for the maintenance of honest signals by the handicap
principle; however, in some cases, for example if there is no
conflict of interest between the signaller and the receiver
and the communication is cooperative, the signal may
convey reliable information even if signalling is cost-free.
An example of an honest signalling system
Hygrolycosa rubrofasciata is a small lycosid spider which
occurs in bogs throughout northern Europe and western
Siberia. In early spring, males advertise themselves to the
females by drumming dry leaves with their abdomen. The
drumming is clearly audible to the human ear from several
metres. Male drumming rate is positively correlated with
male viability, and is highly condition-dependent (Kotiaho, 2000). Drumming has been found to be costly to
signallers, in that it takes considerable energy to produce
and also increases the risk of predation. Moreover,
simultaneous manipulation of both the signalling rate
and the condition of individuals has shown that drumming
rate is more costly to those individuals in poor condition
than for those in good condition (Kotiaho, 2000). These
results clearly show that, in H. rubrofasciata, male
drumming rate is an honest signal.
H. rubrofasciata females use male drumming signals to
choose their mate, and prefer those males with the highest
drumming rates (Kotiaho et al., 1996). The females do not
derive direct benefits from their mates, but the information
that females receive from male signals may reveal heritable
viability, in that the offspring of males with high drumming
rates survive better than those of males with low drumming
rates (Alatalo et al., 1998).
Deceptive signals
We all know the story of the boy who ‘cried wolf’ when
there was no wolf around, who was then eaten by a wolf
because no one believed him when he was telling the truth.
In the same way as the boy in the story, false signallers are
ignored and are selected out in nature. There are, however,
some signals that are deceptive, in that they cause the
receiver to behave in a way that is beneficial only to the
signaller. This can occur when the deceivers are very rare
compared with honest signallers, or when the cost of
ignoring the signal, whether honest or not, is sufficiently
high that the receiver should always pay attention to the
signal.
Batesian mimicry: an example of a dishonest signal
Prey use warning signals to inform predators that they are
inedible. It is advantageous for both predators and prey to
use these signals, as the prey avoid being eaten and the
predators avoid eating prey that have detrimental fitness
effects, and could be deadly poisonous. Thus the cost of
ignoring these signals is potentially very high for predators,
which allows some species to display warning signals
without being unpalatable. This phenomenon was first
described by the nineteenth century naturalist Walter
Bates, who described a striking similarity between different
species of conspicuous butterflies in the Amazon basin
(Bates, 1862). By copying the same colourful warning
patterns of unpalatable species (referred to as ‘models’),
palatable ‘Batesian mimics’ escape predation, because
predators learn to avoid the unprofitable models and
cannot discriminate between them and the mimics. In this
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Signalling and Reception
way, the receiver is deceived, as Batesian mimics are
potentially edible prey. However, if the mimics become too
abundant, predators are likely to sample both edible and
inedible species while learning to avoid them, and the signal
will lose its meaning to receivers; therefore, Batesian
mimics should always be rare relative to the abundance of
their models.
Audience effect
One other interesting influence that changes signaller
behaviour is the size of its potential audience. The audience
of a signaller includes the intended recipients, and also all
other individuals that can potentially receive and use the
signal (see also Eavesdropping, below). A good example of
the audience effect is where signallers only signal if
conspecifics are present. Experiments investigating alarm
calling in male chickens show that males are more likely to
give alarm calls in response to aerial predators if there are
conspecifics present than if they are alone. This suggests
that, because of the risk of being attacked, it is only
advantageous for these males to make this call when there
are receivers to hear it, especially if those animals are
related. The audience effect may influence other behaviours of an individual, and consequently this term does
not refer exclusively to signalling situations. For example,
male budgerigars have been found to be more likely to
engage in extra-pair courtship and copulation when their
mates are not observing such behaviour. Thus, the
behaviour of the signalling individual can be influenced
by which receivers are present. The next section considers
the role of receivers in the evolution and design of signals in
more detail.
survival by being designed to be easily detected, learned
and avoided by predators.
The perceptual abilities of receivers have a significant
impact on signal design. First, the signal has to be sent
within the sensory limits of the receiver in order for it to be
perceived at all. The sensory systems of animals vary: for
example, birds can perceive ultraviolet wavelengths of light
to which humans, and most other mammals, are blind and
cannot see. In fact, avian visual systems are more sensitive
to colour than those of many mammals, which may explain
why birds often use colourful signals, whereas many
mammals use olfactory or acoustic signals. Second, signals
have to be detected by the receiver against environmental
background noise; for example, acoustic signals need to be
heard over other sounds, perhaps the running water of a
river or the wind rustling the vegetation. Many signals are
therefore highly conspicuous, which increases the likelihood of the intended receiver detecting the signal, but of
course also increases the risk of other animals also
receiving the signal. The level of detectability of a signal
may be considered a trade-off between ensuring the
signaller’s target receives the message while reducing the
chance that the information gets into the wrong hands (see
Eavesdropping, below). Finally, once the signal has been
detected, the receiver has to recognize the signal and
discriminate between signals that are similar. This may
involve the receiver having to learn and remember the
meaning of the signal, so, again, features of a signal that are
easily remembered will be selected for by receivers.
Receivers exert strong selection pressures on signallers
to produce signals that they can readily perceive, and
signallers benefit from their signals being more effective at
producing the desired response from receivers; however, as
mentioned above, it is not only the intended receivers that
affect signal design, but also those animals that eavesdrop.
Signal Design and Receiver Psychology
So far, we have only considered the ‘strategic’ design of a
signal, i.e. how a signal transfers information to receivers,
and how that information is, on the whole, reliable and
honest. There is another aspect to signalling, as signals are
also designed to transfer this information in an efficient
way, i.e. in a way that makes it easy for an intended receiver
to perceive the signal. This has been termed signal ‘efficacy’
(Guilford and Dawkins, 1991), and it can be thought of as
being how the signal is designed to transfer its message. To
understand the evolutionary pressures acting on signal
efficacy, we need to consider the environment in which a
signal is emitted, but also the sensory systems and
psychology of receivers. ‘Receiver psychology’ is likely to
have been important in signal evolution, selecting for those
signals that are easier to detect, recognize, discriminate,
learn and remember (Guilford and Dawkins 1991). A good
example of signals that enhance their efficacy are conspicuous warning signals that increase the chance of prey
4
Eavesdropping
The Concise Oxford Dictionary defines ‘eavesdrop’ as to
‘listen secretly to private conversation’. Of course, this
definition applies to human communication, but the term
eavesdropping is used in a similar way to describe the
situation where a third animal (neither the signaller nor the
intended receiver) receives the signal and obtains information from it. Eavesdroppers can be conspecifics but,
perhaps more commonly, eavesdroppers are from other
species, and indeed are often predators or parasites using
signals to locate their victims. A good example of this has
been found in studies of Gryllus field crickets and their
parasitoids. Male field crickets produce acoustic signals by
stroking their modified forewings together, which serve as
sexual signals to attract females. Field crickets are
parasitized by parasitoid flies (Ormia spp.) and it has been
shown that these flies find their cricket hosts by acoustically
orienting towards their song (Zuk et al., 1998). Thus, the
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Signalling and Reception
parasitoid flies are eavesdropping on the male sexual
signals that are intended for the female crickets. In cases
where eavesdropping is costly for the signaller, as in this
example, signallers have evolved adaptations that minimize the chance of signal detection by eavesdroppers, or
prevent it altogether. One good way to do this is to use a
signal that their predators cannot perceive; for example,
nestlings of bird species that are prone to nest predation use
higher frequency and lower amplitude pecking calls than
other species. These acoustic features make it much more
difficult for the predator to find the nest.
Sensory exploitation and sensory bias
Although receiver psychology can influence the design of a
signal, it can also be ‘exploited’ by signallers. ‘Sensory
exploitation’ occurs when signallers take advantage of
preexisting sensory properties or biases that have evolved
in receivers for reasons unrelated to communication. This
has been proposed as a mechanism by which sexually
selected traits might evolve, with a preference for a
particular trait occurring in females before it actually
evolves in males; obviously such a trait will have a strong
selective advantage through female choice (Ryan, 1998). In
theory, there are good reasons why sensory exploitation
should be common, but as yet we have not enough
empirical evidence to assess the general importance of
sensory exploitation in the evolution of signalling systems
(Johnstone, 1995). One of the best examples for sensory
exploitation comes from studies on the túngara frog
(Physalaemus pustulosus) species complex. In this group
of frogs, some species produce calls consisting of two
different components, while others produce calls with only
one component. If the mating call of a male from a species
that has only one component is digitally mastered to
contain two components, females now prefer the new call
with the additional component. Thus it would appear that
females prefer a call with more components if it were to
evolve in this species. In fact, if we look at the evolutionary
history of this group of frogs, the male calls become
increasingly complex as the species evolve. This confirms
the results of the experiments, and gives strong support for
preexisting sensory biases in females and sensory exploitation by males (Ryan, 1998).
Signalling in Plants
Communication is often thought to be characteristic of the
animal kingdom but signalling also occurs in plants; for
example, the colours and scents of flowers in animal
pollinated plant species are clear signals that have evolved
to attract pollinators. The flowers offer pollen and nectar
rewards to foraging pollinators, while at the same time
benefiting from these foraging animals when pollen is
transferred between flowers, ensuring their reproductive
success. In most cases the signal of nectar availability is
honest, but there are some plants that deceive pollinators
and do not have nectar (Nilsson, 1992).
There are some other well-known cases of deceptive
signalling in plants; for example, carnivorous pitcher
plants (Rafflesiaceae) use ultraviolet and olfactory signals
to deceive insects into approaching them, when they are
then trapped and digested. Another interesting example is
found in some orchids (Orchidaceae) which produce
flowers that resemble the body and crossed wings of a
particular female insect, tricking male insects into ‘copulating’ with the flower. The orchids have evolved not only a
visual resemblance to female insects but the flowers also
emit chemical compounds that are identical to those
produced in the pheromonal secretions of the receptive
female insects (Nilsson, 1992). The insect does not gain
anything from the orchid but with the fraudulent signalling
the orchid may achieve pollination.
Animals may not be the only receivers of plant
signals: there is some evidence of signalling between
plants. For example, when sagebrush plants are
experimentally clipped, they release a pulse of a chemical
that functions as a volatile signal capable of inducing
resistance to herbivory in neighbouring undamaged wild
tobacco plants (Karban et al., 2000). Although this does
not show that these chemicals have explicitly evolved as
signals, it does show that plants can potentially perceive
and respond to chemical cues from other plants. These
examples show that signalling and communication are
common phenomena not only among animals but also
among plants.
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ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net