Animal Communication

Few have supposed that living species other than Homo sapiens possess
methods of communication that shed much light on issues that arise from the
study of human language and linguistics. Methods of communication used by
animals have however received attention from those interested in describing and
accounting for animal behaviour itself. That there often remain implicit analogies
with human exchange of information is indicated by the difficulties of defining
which sorts of animal behaviour should be counted as communicative and which
not.

1. Definition of Animal Communication

It is not difficult to select examples of behaviours which obviously qualify
as some sort of communication — such as warning cries, or the release of
chemical attractants. There is little agreement, however, on a formal definition to
cover less obvious cases. The widest includes any method by which one animal
(or cell) demonstrably influences the behaviour of another (Wilson, 1975). This is
straightforward enough, but it is usual to qualify it in ways related to intuitive
notions of functional specialization. The natural world is sustained by one animal
eating another: an act of this kind undoubtedly alters the behaviour of both, but is
certainly not primarily communicative. Predation can easily be excluded, and for
most purposes it is convenient only to consider interactions between members of
the same species, although symbiotic relations between different species, and
deception of predators by prey, may involve interesting specializations. A narrow
definition would focus attention on behaviours which it is reasonable to suppose
have been selected because of the benefits to both the sender and the receiver of
the transient messages thus conveyed. Mechanisms which appear to have evolved
particularly to serve communicative and therefore social functions, such as
vocalization and the release of chemicals, and clearly of most interest. but the
benefits which they bring are not always easy to determine, and when they are the
distinction between transient and sustained signals is not always supported. It is
arguable that any frequent social interaction between conspecifics will come to
involve communication, but many would wish to exclude such apparently trivial
examples as the avoidance of collisions. As an alternative to defining
communication, it may to sufficient to discuss uncontentious examples, and to
examine their functions.

2. Functions of Animal communication

The over-riding explanatory principle for animal behaviour is that of the
theory of evolution, most often expressed not just in terms of the advantage of the
individual, but by reference to the individual's genes. Behaviours under genetic
control persist only if they optimise transmission of the individual's genes to the
next generation. The initial presumption is that of selfishness, and this does not
suggest that communicative mechanisms which provide mutual benefit should be
at a premium. Communicative activities, if specialized, must entail costs of time,
energy and computational effort to both sender and receiver: if both are selfish
whey do they not confine themselves to securing individual comfort and well
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being? General theories of social behaviour supply two kinds of qualification. The
first is kin-selection. In genetic terms selfishness can encompass parental care, and
indeed more extreme forms of self-sacrifice in return for the survival of sufficient
numbers of close relatives. Observations of interactions between parents and
young form a substantial part of the discipline of ethology — the approach to the
study of animal behaviour which has supplied some of the conceptual framework
for analyses of communication. The second qualification is "reciprocal altruism",
which can be mathematically justified, but is suggested partly because of
observations of elaborate social interactions not otherwise readily explicable. The
most selfish individual should co-operate with others if its own benefits are
increased as a result, which can happen if favours are returned, or if collective
activities benefit all co-operators more than cheaters or individualists.
The direct relevance of these corollaries of evolutionary theory to the
analysis of animal communication is that they both require some kind of
individual and group recognition. If parental care is to be justified by kin-selection
it ought to be directed at the correct offspring: in relatively solitary species a
minor constraint, but a major one in those breeding in colonies or flocks. Where
group behaviour is co-operative, recognition of particular individual conspecifics
is implied by the rules of reciprocal altruism, while where groups are formed as
less complex aggregations, presumptively on "safety in numbers" grounds, there
needs to be at least a sensitivity to whom else to aggregate with.

2.1 Recognition.
A first function for communication is therefore recognition of species:
more detailed social interactions for a variety of purposes need to be with
conspecifics. Species recognition may be in many cases built in to sensory
systems, but in some birds and mammals infants may acquire it from interactions
with their parents, this process being known as imprinting. Acquired recognition
is more obvious when local group membership is a factor in the details of
communication, as for example with local dialects of vocalization (some song-
birds) or local variations in group odour (some rodents). Within communities of
social insects caste distinctions are typical, and within small groups of birds and
mammals there is usually recognition of group members in terms of size, age and
gender, and often also, as in the peck-orders of chickens and in other dominance
hierarchies, recognition of each individual by any of the others. Generally it is
assumed that animal communicative behaviours are genetically determined, and
common to all members of the same species. Paradoxically however, it can be
demonstrated in higher vertebrates, if not in insects, that one of the functions of
the innate mechanisms is to enable individuals to acquire information which is
peculiar to their own circumstances of life, which can include recognition of the
identity of unique individuals, and membership of local groups. Even recognition
of species membership may be learned, as with imprinting.

2.2 Courtship and mate selection

Even the most solitary species must engage in the social interactions
required for sexual reproduction (parthenogenesis is extremely rare). Evolutionary
theorists from Darwin himself onwards have deduced that mate choice is likely to
produce via sexual selection effects not predictable from the more humdrum
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necessities of day-to-day survival. Hence the antlers of the stag and the tail-
feathers of the male peacock, and the behaviours that accompany these. Dispersed
species must communicate at a distance to bring males and females into
proximity. Especially where several similar species co-exist in the same
geographical area (not unusual for insects) fine distinctions between species-
specific signals need to be made. Some species differences may be very
straightforward, as with the different frequencies of calls made by species of
cricket which differ in size. In other cases there appears to be more specialization
in the evolution of particular signals, as in the patterning of acoustic messages in
some other species of crickets, and more notably in bird song. The flashing of
different species of firefly is also distinguished by temporal patterning. A further
source of differentiation of species (and individual) recognition in mate selection
lies in sequential "handshaking" between members of a pair. Male fireflies
typically discriminate females of their own species by the precise time-delay
between their own signal and the female's flash in response. Detailed sequential
ordering of male-female interactions is common in courtship involving visual
recognition, with an example being found in the ethologist Tinbergen's classic
studies of the "zig-zag dance" during which a male stickleback leads a female
back to his nest for spawning.
The degree of social interaction involved in mate selection varies from a
single act of spawning to much more protracted shared parental activities, which
are common in birds, where a male and female often pair permanently, or for
several seasons, in some species remaining together throughout the year, but in
others separating outside the breeding period. Among mammals similar "pair-
bonding" occurs in for instance beavers, when dam construction and/or
maintenance is shared, in wolves and other canids, in which food is brought to
pregnant or nursing females and young, and gibbons, where the functional reasons
for the pairing are less obvious. Clearly methods of individual recognition, and
signals for shared activities (e.g. turn-taking in incubation) are necessary in these
cases. Sometimes the pair engage in elaborate gestural "ceremonies" during
courtship, as in Great Crested Grebes, and these may contribute to both species
and individual recognition via the visual modality. Individual recognition by smell
is fairly standard in terrestrial mammals, but the use of all the sensory modalities
available to any species is to be expected. Striking examples of vocal
communication occur in species which use "duetting" or antiphonal singing
between mated pairs. In East African shrikes, which forage together in dense
foliage, each pair develops some idiosyncratic patterns among the several heard in
antiphonal singing, while other patterns represent geographically localized
dialects. Of seven species of pair-bonding lesser apes (gibbons and the Siamang)
all but one have antiphonal singing between pairs (the other has lengthy all male
and all female chorusing between adjacent groups). In two of these six species the
male and female contributions never overlap. In the other four they do: in one
species the male produces similar sounds to the female but at a lower pitch; but
with the rest the male makes limited additions to a more complex female song.

2.3 Aggression and Threat

In deer and peacocks and many other species there is competition among
males for access to females, along with male self-advertisement. Much but not all
bird song is in this category. Aggression is of course also found in relation to
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disputes over territory and food. It is communicative in the specialized sense in so

far as the interaction in the form of assertive calls and snarls, or gestural displays
and postures, as alternatives or additions to direct physical struggle, which is
usually the case. In highly social species including wolves and many monkeys
aggressive displays may be finely tuned according to the status of the interacting
individuals in the group structure, and gestures of submission and appeasement
from subordinates may be as important as those of threat from the more dominant.
In these instances communication is usually over short distances, and indeed may
include tactile sensation. Threat between neighbouring groups or between
dispersed individuals usually involves greater distances and is well-served by loud
vocalization, or territorial scent marking. It has been shown that bird song (even
from a loudspeaker) deters other males from entering the vicinity of its location.
The roars of the howler monkey can be heard a kilometre away, and may
reasonably be assumed to have a territorial function. The elaborate chest-beating
display of the male gorilla, which includes hooting, the shaking of branches and
the slapping of the ground, is often directed at a neighbouring troop but is also
probably related to the maintenance of dominance relations with closer observers.

2.4 Alarm and Distress

A more benign form of social signalling is anything which serves as a
warning to others of danger from predators. There is an explanation for pure and
simple social aggregation from the benefits to any single individual in terms of
predator avoidance. But a selfish individual, on detecting danger, might seem best
advised in the short term to make a disguised retreat, and indeed to maximize
rather than reduce the disadvantage to its conspecific competitors. In groups with
a high degree of consanguinity warning to others, or indeed self-sacrificial
defence of them, would be explicable in terms of kin-selection, and this is
obviously the case for the social insects (which have single breeding queens for
each community, and sterile workers; and, except for termites, have complicated
increases in consanguinity because all males come from unfertilized eggs). Lesser
degrees of consanguinity may contribute to the prevalence of alarm signals in
small groups, particularly in monkeys and apes, where longevity, long-term group
coherence and mutual dependence may foster reciprocal altruism. It has been
suggested that in other cases giving an alarm call may in fact directly benefit the
transmitting individual. That acoustic warnings (as opposed to alarms which elicit
defensive aggression by the group) have evolved so as to be difficult to localize
indicates that they are not without risk. However, it may to the advantage of an
alerted individual to elicit collective evasive action — for instance, an individual
bird in a ground feeding flock would probably be unwise to fly off on its own if it
sights a hawk. Alternatively, signals given in reaction to predator proximity which
are ostensibly altruistic may not be what they seem: it is now believed that the
leaping ("stotting") of gazelles when fleeing advertises the vigour and alertness of
the fleeing individual to the predator, rather than the presence of the predator to
alternative prey. For whatever reason, apparently communicative reactions to
predator presence are common, and are sometimes utilized by species other than
that of the transmitter. They may differ in the same transmitting species, according
to circumstances, including predator type. Mobbing calls in birds differ from other
alerting or warning calls, in particular by being easy to localize, and the different
cries made by vervet monkeys in response sightings of leopards, hawks, or
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pythons cause others to run to trees, to look up, or to look down, respectively. It is
believed that infants learn the individual meanings of these calls, and
experimental evidence suggests that fear of both natural and artificial objects is
induced in both primates and birds if the young observe adults making alarm
reactions to their presence.
Vocal or chemical signals elicited by fear or pain may function as warning
messages, but as a special case, infant distress signals clearly function to elicit
parental assistance. In experiments mother rats, cats, and hens react to the
vocalization of a misplaced infant by taking steps to retrieve it (the specificity of
the response in hens having been demonstrated by the fact that they ignore
offspring visible distressed but acoustically isolated under a glass bell). Much less
common than signs of distress in infants are "satisfaction messages" but the
familiar purring of domestic cats, and similar sounds produced by only the young
of wild carnivores, are sometimes given this description. As these sounds are
accompanied by vibrations it is thought they may function to confirm bodily
contact.

2.5 Signals related to feeding

The most celebrated example of animal communication is the system by
which foraging honey bees convey to their fellows information about the location
of recently used food sources (see SPECIALIZED ARTICLE: in related bee species,
and many species of ant, individuals lay olfactory trails to known food sources
which are subsequently used by other colony members). But this kind of specific
communication of the location of distant food sources is known only in the social
insects. The most general form of communication in this category is simply the
visual observation by one animal of another feeding, which has behavioural
effects which are readily obvious in seagulls and other flocking birds. There is
rarely any suggestion that the feeding animal emits signals with a specialized
communicative role. However among social primates "food finding calls" have
been identified, such as the low grunting of the chimpanzee when it discovers
highly preferred food such as bananas or palm fruit. Food sharing occurs within
chimpanzee groups and the rarity of food-finding signals is undoubtedly related to
the fact that feeding is usually competitive. In chimpanzees and baboons there is
occasional hunting of the young of other species by males, with its products being
shared with females and infants, among whom there is the intuitively
understandable begging gesture of holding out the hand, palm upwards. In wolves
and other canids meat sharing is routine in family groups, the reactions of the
young, such as licking the muzzle of the returning parent, often being required to
elicit regurgitation.
A similar pattern is very common in birds, and the interactions between
parental feeding and the begging responses of nestlings was an early focus of
attention for ethologists. A gaping response, with vocalization, occurs in the
nestlings of many species, and the probability of being fed is related to the vigour
of the begging. In gulls, nestlings peck at the parental beak to elicit regurgitation,
and the precise visual features of the parent's head and beak which act best as
stimuli for these pecks have been studied by the use of models. In fowl, where the
young feed themselves from birth, there are usually special calls used by both
parents to attract the young to food, and these are sometimes also included in
courtship feeding of females by males.
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2.6 Co-ordination of group behaviours

Flocking, herding and schooling require that individual animals influence
one another, but these kinds of co-ordination may occur without the emission of
specialized signals, as long as individuals are sensitive to the movements of
others. Thus social facilitation is sometimes distinguished from co-ordination via
known communicative mechanisms. However, in most social species, especially
of birds and mammals, many more communicative behaviours are observed than
can be accounted for in terms of the specific functions of mate selection, alarm
calls and so on listed above.There are of course other functional categories, such
as group migration and co-operative hunting, which have not been listed. Another
area is juvenile play, in carnivores and primates, which is recognizable from
specialized gestures, cries and facial expressions, and which is assumed to have
some functions which are related to socialization. But there are also more general
categories of behaviour which may serve vaguer functions such as social cohesion
and affiliation. Thus species are said to use, for instance, "greeting displays" and
"bonding messages" (vocal chorusing being an example of the latter). As the last
point in this section on functions of communication therefore, one should note
that although functionality is an underlying assumption it is by no means the rule
that the functions of any agreed instance of animal communication can be readily
identified.

3. Channels of communication
Channels of communication map on to the available sensory modalities,
usually taste, smell, touch, vision and hearing. (These cover everything except the
production and detection of electrical fields, which is peculiar to a few species of
fish.) There are issues surrounding the advantages and disadvantages of each
modality. The following factors vary: the cost in time and energy of coding and
decoding signals, especially in relation to the effect on other concurrent activities;
the distance signals need to carry; the ease with which the location of the
transmission can be fixed; and the capacity of the channel in terms of the rate at
which information can be transmitted.

3.1 The chemical channel

The substances used as signals are known as pheremones. These are
secreted as liquid and transmitted as liquids or gases. Pheremones may be smelt as
gases at great distances, but can also operate locally. The distinction between taste
and smell is not always clear-cut, especially in insects, although olfaction is
obviously the main route for chemical detection of signals in land mammals. An
important aspect of pheremones in both mammals and insects is their deposit as
trails or markers — in this case the individual which transmits the signal can be
distant from the receiver in both space and time. However, the airborne dispersal
of chemical attractants provides an efficient mechanism for bringing together
dispersed individuals of opposite sex, and the precise compounds used are known
for many species. The female silkworm moth secretes one termed bombykol:
males are sensitive to just a few molecules of this substance and may be attracted
from distances of several kilometres. In higher concentrations, for moths and
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some other insects, full male sexual behaviour is elicited towards any object
strongly marked with the scent.
Chemical transmission of information is in some ways primitive, as it can
operate at the cellular level, and it has similarities to the internal communication
between bodily organs via hormones. However, the complexity of chemical
communication reaches its peak in the social insects and mammals. Over 100
species of mammal are known to have anal glands for adding distinctive
pheremones to faeces, and many mammals possess a number of specialized scent
glands. A deer, for example, can transmit scents from glands on the legs and head
through the air, can also mark trees and twigs from the same glands, and has other
glands on the feet for leaving scent trials on the ground. For the most part
transmission of signals by this sort of scent marking is not cognitively demanding,
though interpretation on reception may sometimes be less straightforward. Some
insect pheremones disperse very rapidly, but typically chemical signals have the
advantage of being long lasting, and the corresponding limitation of carrying a
relatively low rate of information transmission, by comparison with acoustic and
visual signals. Chemical communication is nevertheless responsible for complex
social organization: the societies of ants, bees and termites are ordered very
largely by pheremones, and scent in mammals is used for several kinds of social
identification. Although the initial reception of chemical signals may be regarded
as less psychologically demanding than the decoding of auditory or visual cues, it
may be noted that tracking the location of a distant source of pheremones presents
problems, even for insects, whose solution requires at the very least a combined
sensitivity to concentration gradients and wind direction.
There appears to be no evidence for the use of olfaction for social
communication in birds, although olfactory cues may be involved to some extent
in avian homing and migration. Although whales are mammals, they make
minimal use of chemical communication (see section 3.4). Old-world monkeys
and apes rely less on olfaction that most other terrestrial mammals: pheremones
certainly influence sexual behaviour in some species, but there is a marked lack of
specialized glands and scent-marking behaviours in higher primates. However,
although in modern human societies the possible functional roles of natural social
odours are culturally inhibited, humans, like other primates, still possess apocrine
sweat glands. These are not important for cooling purposes (as they are in non-
primates: in primates the epicrine glands serve for thermoregulation) but are
responsible for body odours typically judged as unpleasant. The apocrine glands
only become active at puberty, are highly responsive to stress and excitement, and
are larger in males – suggesting that they originally had some social and therefore
communicative functions.

3.2 The tactile channel

The limitation on communication by touch is clearly that of distance. It is
nevertheless widely and perhaps inevitably part of close-contact social and
emotional interactions between animals. Hugging, kissing, caressing and biting
may take specialized forms in sexual contexts, and elicit specialized reactions:
indeed in many mammals other than primates ovulation and/or the hormonal
changes associated with pregnancy are induced by the tactile consequences of
copulation. Physical contact is also an important element of the social relationship
between offspring and parent in most mammals.
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A particular case of tactile stimulation associated with a less obvious

social process occurs in mutual grooming. This might be thought to be a purely
utilitarian example of reciprocal altruism, and indeed this may be its functional
origin, but the grooming or preening of one animal by another is often interpreted
as a ritualized form of conciliation or social bonding. Monkeys and apes spend a
surprising amount of time meticulously picking parasites and dirt from each
other's hair, and, as attention is frequently (but not always) concentrated on parts
of the body which the recipient would have difficulty reaching, this must in part
be a matter of co-operative cleaning. However, the timing of grooming bouts, and
their distribution between individuals placed in dominance hierarchies and other
social sub-groupings, suggest that the motivation for grooming is inversely related
to aggression. (It is difficult to determine the extent to which the sensation of
touch is important in this, since the postures and gestures involved in soliciting
and proffering grooming are more readily observable).
Apart from its prevalence in primates, social grooming between adults is
extensive in rodents and occurs intensively in several bird species. Its social
function in carnivores may be indicated by the propensity of domestic dogs and
cats for licking the hands and faces of their owners.

3.3 The visual channel

The emission of light in dark environments by fireflies, other invertebrates
and deep sea fish provides a clear example of an activity which is specialized for
communicative purposes, but overwhelmingly the use of the visual channel means
recognition by sight in daylight. There is here an unmistakeable ecological
constraint on choice of channel: visual communication is useful only when
animals can easily see each other, which is normally by day, with uninterrupted
sight-lines. The acoustic and olfactory channels do not have this limitation. And
although people can (in daylight) often identify each other by appearance and
gesture at distances from which it is impractical to converse, the visual channel in
most species operates best at short distances, by comparison with chemical and
acoustic cues.
Visual specializations for social communication are nevertheless common.
Most obvious is the evolution of distinctive features or markings as aids to
species, gender, and individual identification. Visual appearance might of course
be used for species identification without features having evolved for that purpose
(an elephant is large, and has a trunk, for other reasons) but many species have
colouring or bodily appurtenances such as crests which are specialized for
communicative functions. These may be permanently fixed, or variable according
to age or season, and the relative permanence, at little or no cost in time and
energy to the transmitting individual, provides and advantage for the visual
channel. However there is sometimes more interest in transient communicative
acts, construed as the sending of signals, precisely because these involve a greater
behavioural investment on the part of the sender. There is no shortage of examples
within the visual channel. Behaviours thus categorized are often termed displays.
In fish, reptiles and cephalopods (octopus and squid) they may include rapid
changes in skin colour or marking. In mammals, particularly carnivores and
primates, visual displays include changes in facial expression, although these are
often accompanied by vocalization. In social lizards changes in the appearance of
the head by extensions and colourings of dewlaps, crests and frills are normal. But
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any part of the body may take part in visual displays. Lizards have back arching,
tail lashing, head bobbing and circular forelimb waving for aggressive and
submissive gestures. Posture, gait, and gestures via movements of the extremities
can be identified as social signals in a wide range of vertebrate and invertebrate
species which have the ecological and perceptual opportunities for the detection of
visual messages.

3.4 The acoustic channel

Clearly, acoustic forms of animal communication have greater superficial
similarity to human speech than chemical or visual signals. Apart from this, this
acoustic channel shares with olfaction the virtues of broadcast transmission over
considerable distances, and availability in the dark or when lines of sight are
interrupted. It is arguable that in many species (songbirds, crickets) hearing as a
sense must be specialized for the purpose of social communication, as opposed to
food seeking and predator avoidance. In others, by contrast, (bats and dolphins)
the acoustic sense is utilized as the major avenue for prey detection — by echo-
location. This is sometimes considered to be "solipsistic communication", but
falls outside the present social perspective. Many other predators (cats, owls) have
highly developed hearing which is used for detecting sounds produced by prey.
The production of sounds for the purposes of echo-location would be one kind of
exception to the general rule that distinctive animal noises will have evolved
because of their advantage in within-species communication. Another category of
exception is the noise of locomotion, and in particular the flight sounds of insects,
which are the inevitable consequences of wing-movements. These sounds are not
usually detectable by flying conspecifics, although the male mosquito has a sense
organ on its antennae tuned precisely to the distinctive drone of the female and
insensitive to the higher pitched flight sounds of other males. This is an example
of an entire perceptual mechanism being specialized for social communication:
another is in a species of tree frog in which males produce a bi-phasic call of a
low-frequency "co" followed by a high-frequency "qui"; the inner ears of the
males being tuned to the "co", which serves as a territorial signal maintaining their
dispersal, while the inner ears of the females are tune to the "qui", as a sexual
attractant. In higher vertebrates the peripheral hearing apparatus is, as far as is
known, exclusively general purpose, but there are often ways in which the central
nervous system is clearly able to selectively process sounds with species-specific
characteristics (e.g. newly hatched ducks being sensitive to the parental calls of
their particular species).
Vocalizations in higher vertebrates, and many courtship noises produced
by fish and insects, are quite obviously specialized ways of sending social signals.
In animals communicative sound production is frequently very effortful: insects
such as crickets produce a large amount of noise in relation to their size, and a
cicada may need to increase its resting metabolic rate by a factor of 20 in order to
sing; some small frogs which increase their metabolic rate while calling by a
factor of 5 have been estimated to expend more than 80% of their total calorific
intake on this activity during a 6-month breeding season. This may be contrasted
with the use of chemical signals, where, since the recipient can be sensitive to just
a molecule or two and air-borne transmission is free, minute amounts of
pheremone are sufficient to produce dramatic effects. This raises the question of
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why the auditory channel should ever be preferred to the chemical for broadcast
transmission.
The presumed advantages of the acoustic channel are in its high carrying
capacity for rapid serial transmission, and in the possibilities for swift and
accurate source localization which, though not perhaps as direct as those for
visual signals, are in general much more favourable than those for dispersed
chemicals. Some of the complexities which may be carried by the acoustic
channel are apparent even in the courtship calls of male frogs, particularly in sub-
tropical species which breed opportunistically after heavy rains. In many of these
species males gather together to make simple sounds in choruses, and often
several different species occupy the same areas. Auditory discrimination of
species-characteristic signals is therefore required of females. Aggregations of
males could be fortuitous if breeding sites are limited, but there is evidence that
the groupings are systematic, the assumption being that the greater volume or
longer duration of a chorus means that dispersed individuals would be at a
disadvantage. This assumption is supported by the finding of highly organized
sub-groups within choruses. There are species in which individuals within a
chorus alternate calls within duos, trios, and quartets, at precise intervals. There
are leading individuals in the sub-groups, and leading sub-groups within choruses.
Thus chorusing is actively synchronised, rather than being the result of the
accidental contiguity of individuals. The balance of advantage to individuals
which supports this collectively organized form of communication is clearly very
complicated to determine, but this is typical of most animal social behaviour.
Frogs are modern amphibians, and their vocalization has evolved in the
context of nocturnal and time-limited (after rains) breeding. Higher vertebrates,
that is birds and mammals, both evolved from reptiles, which as a class post-dates
amphibians. Existing species of reptile are not generally very vocal. However, the
neural organization of the auditory pathways in the reptilian brain is surprisingly
similar to that of higher vertebrates, and the absence of acoustic communication in
many reptiles is therefore likely to be due to ecological factors which favour
visual or olfactory methods of communication when any is required. A limited
range of vocalization occurs during the courtship and mating of several species of
tortoises and turtles. Use of the acoustic channel as extensive as that of frogs
appears to be confined to the geckos, a large family of lizards distinguished by
nocturnality. Not all geckos are equally nocturnal, or equally vocal, but the family
differs from other reptiles in having an external auditory meatus, and in many
species the cochlea is highly developed. Vocalization in geckos is characterized as
chirruping, or multiple chirruping, but very little is known about its behavioural
functions. Most species are communal and territorial, and some vocalization
probably functions as an assertion display for territorial defence. Loud continuous
chirruping during a "dusk chorus" is heard in the gecko Ptenopus garrulus
garrulus, when individuals emerge from their burrows.
Thus in amphibians and reptiles acoustic communication seems to be
clearly correlated with nocturnality, but this correlation does not hold for other
taxonomic groups. Among insects diurnal sound production occurs in
grasshoppers and cicada, and the most elaborate use of the acoustic channel is of
course in birds, almost all of which are diurnal, but which are usually too small to
be easily visible at a distance. Owls and nightingales vocalize at night, and the
most intensive singing in song-birds takes place at dawn and dusk. But enough
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avian (and mammalian) vocalization takes place during the hours of daylight to
dispose of the notion that nocturnality is the only factor favouring the use of the
acoustic channel. There may however be some trade-off between visual and
auditory communication depending on the ease of visibility. In most birds vision
and hearing are both well developed, while olfaction is of lesser importance. It has
been suggested that male courtship singing is less elaborate in more highly
coloured species, and there may also be a negative correlation between size and
complexity of vocalization: the song birds (Oscines) which have very detailed
control of the sound producing organ (the syrinx) are relatively small, while larger
and therefore more conspicuous birds tend to produce a narrower range of sounds,
storks being almost mute, and the cries of geese and cranes being notable for
volume rather than variety. Whatever the underlying reason for it, the extensive
use of vocalization in birds raises a number of theoretical issues, in particular the
interplay between inherited and species-specific control of sound-production and
the development of individual variation by within-species learning and cross-
species mimicry (see below).
The original mammals were nocturnal, and as a vertebrate class mammals
are notable for extensive reliance on olfaction. Apart from primates, mammals
have little or no colour vision, and no retinal fovea for high visual acuity, and
therefore have little opportunity to use colour signals and some limitation on very
detailed visual display or markings. As a very rough generalization, reptile
communication is olfactory and visual, with little use of vocalization except in
nocturnal lizards, birds have highly developed use of both visual and acoustic
channels, and mammals use all four channels with the emphasis, if any, on the
chemical. This is clearly an over-simplification, and primates (monkeys and apes)
are in this context closer to birds than other mammals, since they share with them
foveal colour vision, and a reduced reliance on social odours. Colour is in fact of
little importance in primate social signalling, apart from one or two species of
monkey (and perhaps human blushing). But social primates such as rhesus and
vervet monkeys, chimpanzees and gibbons have a wide range of vocalizations, as
well as making considerable use of the visual channel for gestural and postural
displays, and for facial expression (see SPECIALIZED ARTICLE).
Whales and dolphins (small toothed whales) are even clearer exceptions to
the rule that mammals make extensive use of chemical communication, since
baleen whales (e.g. the Humpback, Sei and Rorqual) are considered to have very
little sense of smell, and toothed whales (Sperm, Killer and all dolphins) none at
all, since they have reduced or entirely lacking olfactory bulbs (and there is no
evidence to suggest that their sense of taste functions to detect water-borne
chemicals). In addition to lacking an acute sense of small, many cetacean species
have poor vision, as they feed in deep water, or under ice, or are nocturnal (the
best known dolphins feed near the surface, and can see reasonably well, but the
Gangetic river dolphin is nocturnal and almost blind). Therefore most whales
must rely heavily on audition for any form of distant social communication. The
picture is complicated because many toothed cetaceans also emit sounds for the
purpose of echo-location of prey, but since most species are highly social, it is
usually assumed that sound production and reception also play a part in
communication. Detailed evidence of the precise functions of particular sounds is
sparse for species other than the bottlenosed dolphin. Here a distinction can be
drawn between pure tone whistles or squeals, which serve for individual
 12

identification and other social purposes, and pulsed clicks which are primarily for
echo-location. However, many different categories of pulsed sounds have been
identified, whose behavioural function is unclear. An extremely wide range of
sounds other than clicks or whistles have been recorded in other species, such as
the baleen humpback, whose song carries vast distances, and the odontecete
Beluga, or "sea canary." (See SPECIALIZED ARTICLE)

4. Theoretical Issues in Animal communication

The description of animal communication given so far has inevitably
encompassed some underlying theoretical assumptions about its behavioural
functions, and the relative advantages of the various sensory channels. There are
however some additional points to be made.

4.1 Evolutionary development

Several theoretical ideas about the evolution of communicative
mechanisms go back to Darwin's The Expression of the Emotions in Man and
Animals (1872). In this work he put forward three general principles which are
reflected to some extent in more recent analyses of the topic. His first principle
was that of "serviceable associated habits", which may be construed as the notion
that actions which initially evolved for other reasons may come to be selected for
more specialized communicative purposes. One of Darwin's examples was the
laying back of the ears in cats as part of the facial expression of fear. This,
together with narrowing of the eyes, he supposed had initially a purely protective
function. In this case it is not clear how supposed original and later
communicative functions can be separated but modern ethologists employ the
similar concept of ritualization on the basis of many other examples. For instance,
behaviours which form part of courtship, such as mutual feeding in birds, are
often similar to those which occur in other contexts — in this case parental
feeding of the young. The concept of ritualization implies that already present
behavioural units may become incorporated into communicative displays, and
then exaggerated or otherwise altered. It is not of course necessary to suppose that
all forms of communication are ritualized versions of other behaviours – it would
be difficult for instance to account for elaborate vocalization in this way. The
same caveat applies to Darwin's principle of "the direct action of the nervous
system". His example here was trembling, which occurs in both people and
animals under conditions of fear or excitement. The argument is that trembling
movements are a side-effect of arousal and muscle tension rather than the
transmission of a specialized signal. In general, it is necessary to separate the
interests of the senders and receivers of possible messages.

4.2 Discrete and graded signals

The remaining one of Darwin's three principles is that of "antithesis". A
dog's tail indicates happiness when aloft but sadness when lowered between its
legs: in general opposed emotions are expressed by opposite movements. This no
doubt simplifies both the production and interpretation of messages. It also
incorporates the possibility that a continuously varying signal can convey a range
of information: there is good reason to believe that intermediate positions of a
 13

dog's tail convey intermediate emotional states, and there are may other examples,
particularly in facial expression, and gestures which convey an individual's mood.
By contrast, signals are regarded as "discrete" if their production is unvarying and
stereotyped, or if reactions to them occur in an all-or-nothing manner. Those for
group and species recognition may be in this category, such as contact calls in
birds and the flashing of fireflies. Receptive reactions to discrete versus graded
signals may be compared to the distinction between categorical and continuous
perception of human speech, although whether or not variable signals are actually
elicited a wide range of responses is not always tested. Another terminological
variation to refer to "analog" or "digital" signals. It is usually assumed that most
species will use a mixture of discrete and graded signals, even within the same
modality. Discrete signalling, and/or on/off responding to signals is presumed to
have advantages over long distances, or where for some other reason variations
the graded aspects of the received signal may not reflect the targeted aspect of
message content. (In speech. graded aspects such as tone and accent represent
mood and identity, while linguistic information is received discretely). Graded
signalling, if it is reliable, has clear benefits in terms of economy of information
exchange, and is expected to be found in close range, within-group
communication. An example of different kinds of signalling within the same
modality is the song of the European Robin. Songs consist of about 4 phrases,
selected out of a repertoire of several hundred for each bird. All the phrases within
each song are different, and all songs in a consecutive run are different. Variability
and elaboration are clearly at a premium, and presumably have value in
impressing other males or attracting females. However, from experiments using
the play-back of artificially assembled robin phrases, and electronically generated
artificial phrases, it is apparent that an important factor in species-recognition is
the discrete rule that phrases within a song alternate between high and low pitch –
if all phrases are different, and they alternate in pitch, lack of verisimilitude in the
phrases themselves is largely ignored. This contrasts with other species such as
Bonelli's warbler, which has a much simpler song based on the repetition of a
single element, and in which subtle analog changes to the real song element
significantly reduces the responsiveness of listening birds of the same species.

4.3 Communication and ecology

The analysis of animal communication is directed at discovering its
functions, broadly characterised earlier in this article. Variations in modalities
used, and in mapping relationships between signals produced and responses
elicited by them, should in theory be explicable in terms of the details of the
environmental circumstances a given species is adapted to, even though this is
only supported by case-by-case examination. The physical environment clearly
limits choices of modality in the example of the absence of visual communication
in nocturnal species, and more detailed inspection reveals correspondences
between, for instance, the precise characteristics of vocalizations and those most
appropriate for optimal dispersion in given geographical conditions. The social
environment of a species and individuals within it is no less important. For
instance in the example of Bonelli's warbler, above, the fact that transposing its
song upwards in pitch slightly severely reduced responses to it, while
transformation downwards had little effect, is almost certainly because this
species often co-exists with another which has a similar but higher-pitched song.
 14

More general comparisons suggest that both song-birds and forest primates which
need to communicate acoustically over relatively short distances, with
comparatively little "noise" from other similar species, have a larger species
repertoire of calls with greater amounts of individual variation, than those in
which group or species members are more widely dispersed, with greater
likelihood of between-species confusions.

4.4 Inherited constraints and universals

The assumption that animal communication systems have evolved to fit
particular species circumstances leads, other things being equal, to the expectation
that both the structure of the motor and sensory organs employed for these
purposes, and the behaviour-controlling functions of the nervous systems that
control them, will be innately determined. Biologists are not surprised by species-
specific universals. There are however exceptions to this expectation, at least in
birds and mammals. The main category is that individuals in social groups learn to
recognise each other by sight, sound and smell. Learning to produce
communicative signals as opposed to perceptual learning is less widespread, but is
a significant factor in bird-song. Vocal learning of one sort or another is pervasive
in birds and ubiquitous, though not universal, in song birds, for reasons which
remain obscure, but which may include, in varying species: i) evolutionary factors
which favour the establishment of local dialects; ii) benefits to the individual of
increased variability of vocal production, either because of distinctiveness for
recognition or where degree of elaboration of song influences female mate choice
and/or impresses other males. An important distinction within avian vocal
learning is that between within-species imitation (and creative elaborations within
a specific species pattern), and vocal mimicry, where birds such as the
Mockingbird or Starling adopt recognizable parts of other species' calls. For
within-species imitation, conformity to a standard form may reflect in some cases
social proximity in early learning (hand reared parents may transmit human
sounds learned by imitation to their offspring) but experimental evidence for
others has led to the concept of an "auditory template", which enables the young
to identify their own species' song as what should be modelled and elaborated.
Inter-species mimicry, on the other hand, demonstrates, (in approximately 15% of
all species), a part of the language learning device in birds which is more
genuinely a tabula rasa. Its existence remains an evolutionary puzzle, since it
occurs in a wide range of habitats and families, although it is more common in
non-migratory insectivorous species. However, not surprisingly, the only common
factor is that it occurs in birds that are dependent on vocal learning for their own
species' calls, and mimicry may be an extreme case of the usefulness of
variability, as well as serving special cases such as the mimicry of host by parasite
species, and the recording of local or migratory histories.

4.5 The evolution of human language.

Little has been learned about the evolution of human language from the
study of animal communication. Marginally more useful comparisons may be
made possible however, if human language is no longer either a) held to be
entirely culturally determined, or, b), assumed to be substantially and crucially
innate, but for reasons that are fortuitous and non-Darwinian. The case has
 15

recently been made that innate capacities underlying human language must have
evolved by Darwinian processes (Pinker and Bloom 1990), and accepting this
implies that there may be points of commonality between the evolutionary biology
of human language and animal communication systems, even though there are
striking differences in the nature of the end-products.
Viewed from the stand-point of natural history, human language remains
unique in its syntactic and propositional character, and the degree to which it
supports cultural transmission and change. It is also unusual in that its functional
importance is not matched by noticeable evolution of the structure of the
peripheral sensory and motor mechanisms which support it, possibly because it is
an extreme case of a system for a large and highly variable repertoire of low-
energy signals transmitted within groups of individuals at close quarters, rather
than one for broadcasting a fixed set of messages reliably at long distances. It is
not remarkable in having both innate and acquired aspects, but far exceeds any
other natural system in the degree to which sociocultural factors are superficially
predominant. Despite features which are arguably unique products of evolutionary
processes, and many others which clearly post-date biological changes (for
example historical language development, and in particular all aspects of language
that are dependent on its written forms) human language continues to serve some
of the same functions as animal communication systems — identification of the
individual, recognition of gender and group, and the other social functions of
greeting, affiliation, assertion and attachment.

Bibliography
Darwin, C (1872/1965) The Expression of the Emotions in Man and Animals.
Chicago University Press.
Halliday, T R and Slater, P J B (1983) Communication. Blackwell Scientific
Publications, Oxford.
Hart, S. (1996) The Language of Animals. Henry Holt, New York.
Hauser, M.D. (1997) The Evolution of Communication. MIT Press, Cambridge,
MA
Pinker, S and Bloom, P (1990) Natural language and natural selection.
Behavioural and Brain Sciences, 13, 707-784.
Walker, S.F. (1985) Animal Thought. Routledge & Kegan Paul, London.
Wilson, E.O. (1975) Sociobiology. Harvard University Press: Cambridge, MA

See also: (e.g. --- to be added by Subject Editor) COMMUNICATION IN INSECTS; THE
DANCE-LANGUAGE OF HONEY BEES; BIRD-SONG; COMMUNICATION IN DOLPHINS AND
WHALES; NATURAL COMMUNICATION IN PRIMATES; ARTIFICIAL TRAINING
EXPERIMENTS WITH CHIMPANZEES, ETC.

S.F. Walker
[Birkbeck College, University of London, UK]