Advanced Review

Animal communication
Gisela Kaplan∗

Animal communication is first and foremost about signal transmission and aims to
understand how communication occurs. It is a field that has contributed to and
been inspired by other fields, from information technology to neuroscience, in
finding ever better methods to eavesdrop on the actual ‘message’ that forms the
basis of communication. Much of this review deals with vocal communication as an
example of the questions that research on communication has tried to answer and it
provides an historical overview of the theoretical arguments proposed. Topics cov-
ered include signal transmission in different environments and different species,
referential signaling, and intentionality. The contention is that animal communi-
cation may reveal significant thought processes that enable some individuals in a
small number of species so far investigated to anticipate what conspecifics might
do, although some researchers think of such behavior as adaptive or worth dis-
missing as anthropomorphizing. The review further points out that some species
are more likely than others to develop more complex communication patterns. It is
a matter of asking how animals categorize their world and which concepts require
cognitive processes and which are adaptive. The review concludes with questions
of life history, social learning, and decision making, all criteria that have remained
relatively unexplored in communication research. Long-lived, cooperative social
animals have so far offered especially exciting prospects for investigation. There
are ample opportunities and now very advanced technologies as well to tap fur-
ther into expressions of memory of signals, be they vocal or expressed in other
modalities. © 2014 John Wiley & Sons, Ltd.

How to cite this article:

WIREs Cogn Sci 2014, 5:661–677. doi: 10.1002/wcs.1321

INTRODUCTION different ways than was conceivable a few decades ago

that our definitions and ideas about the abilities of
O f all the many research fields and disciplines
involved in the life sciences, communication
has probably received the most attention in decades
animals to communicate have been changed too. For
instance, we now know that vast memory storage can
fit into minute structures, and thus can imagine more
involving innovative research in ethology, physiology,
easily that small brains may not mean small cognitive
psychology, and relevant technological inventions.
capacity. We now have good records of vision,1–3
Indeed, for human society the last three decades
auditory ability,4,5 and olfaction,6,7 as well as research
have represented a communication revolution. In the
results for electrical8 and chemical9 perception and
inventive grid that has been generated, from space
communication in animals.
satellites to computers in the home, from e-mail to
internet, and to social media, a new social and political
virtual reality has been created. The ramifications are
profound. Human communication is practised in such ANIMAL PERCEPTIONS UNDER
THE MICROSCOPE
∗ Correspondence Nevertheless, the road to a very active and highly
to: gkaplan@une.edu.au
successful research field of animal communication
Centre for Neuroscience and Animal Behaviour, School of Science
and Technology, University of New England, Armidale, Australia was not at all smooth. The Descartian view of ani-
Conflict of interest: The author has declared no conflicts of interest mals was anything but conducive for any significant
for this article. probing into animal communication since animals

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 Advanced Review wires.wiley.com/cogsci

were considered to be no more than automatons, and on rereading the literature in preparation for this
responding to the world in preset ways. Strangely, it review.
was probably the discovery of echolocation that her- This review is largely a testimony to the extraor-
alded in some change. Initiated in 1938 by Donald dinary scientific achievements in the field of animal
Griffin and involving the physicist G.W. Pierce, who communication in the last 10 years, providing also an
developed piezoelectric crystals, ultrasound was trans- historical perspective of how the science of animal
formed into frequencies audible to humans and this communication has progressed in concert with sub-
was a significant event for researchers in so far as the stantial technological and neuroscientific advances.
discovery clearly indicated that humans cannot hear The review is subdivided into nearly equal parts,
or see, hear, feel, or touch everything other species moving from definitional problems to vocal behavior
might be able to perceive. In the 1950s, it was dis- generally and alarm calls specifically, and devoting a
covered that dolphins also use echolocation.10 Then, separate section to referential signals, including inten-
in 1953, and of significant scholarly repercussions, tionality. Presenting specific highlights in the field (out
came a substantial critique by the American etholo- of many possible ones) lends itself to illustrating effec-
gist Daniel D. Lehrmann of Konrad Lorenz’s insistence tively some of the theoretical tensions and disagree-
on innate behavior. The paper ‘A Critique of Konrad ments on one hand while revealing the multifarious
Lorenz’s Theory of Instinctive Behavior’ was highly and dynamic nature of the field on the other hand.
important because, as an alternative, he stressed the Theoretical antecedents in light of cognition in com-
role of experience and learning. While highly theo- munication are discussed and a final section addresses
retical, the productive debates that ensued underlie some very recent findings in neuroscience and the way
much of the writing on communication to this day in which cognitive processes are being revealed under
even though arguments and perspectives have changed strict experimental conditions. Concluding remarks
significantly. argue that the field has moved into a new and excit-
We now know that learning is indeed a cru- ing phase to address cognition and communication
cial precondition for much in communication. Living and can do so with confidence because methods have
organisms as small as bees can form memories, are been found that provide a biological basis for cognitive
capable of learning, and can effectively communicate complexity in communication.
on the basis of such memory.11 Moreover, communica-
tion spans a vast range of activities from the simplest
inherent actions and responses to the most sophisti- DEFINITIONAL PROBLEMS
cated processes that presume knowledge of a state of A simple definition of what communication in ani-
mind of another in order to be made. mals actually means is almost immediately difficult.
In view of the wide span of capabilities by which Researchers of different theoretical persuasions have
animals communicate, the field is constantly subject tried to reflect the emphasis of their position in the
to revision and keeps producing large and often fas- definition they have given for communication.
cinating volumes on the subject. In the last 50 years Any definition of communication is a little uncer-
or so, there have been at least as many books pub- tain because of the variables involved. It sounds very
lished on animal communication as there are years. simple: one needs at least two players (A and B), A
Books have been published on specialized means of sending a signal and B receiving it and changing its
communication, such as vibrational,12 ultrasonic,13 behavior as a consequence. However, an utterance
vocal,14 and concerning taste and smell,15 visual,16 that we observe and designate as a signal may not be
nonverbal,17 and gestural18 communication, as well as intended as a signal at all. The individual from whom
focusing on specific classes of animals, such as com- a sound may have emanated may have produced the
munication by anurans or fishes19,20 and many on call for any number of purposes; e.g., a self-directed
communication by primates and birds. For obvious call to map out location as echolocation was presumed
reasons, they cannot all be mentioned. The number to do, a call uttered involuntarily when encountering
of published papers on animal communication is also something frightening or unexpected. This makes the
staggering. original issuer of the call not a signaler while it could
What this review can do is allude to main lines still be a signal to a receiver. Even if it is, in fact, a
of argument and development and provide insights communicative signal (more of that below), points A
about alarm calls as just one, albeit pertinent, example and B may be divided by time and place (Figure 1).
of animal communication, note the present currents The signal may be marred by distortions and
and influences on the field, and provide a few pointers interferences. It may be instantaneous or slow depend-
for future directions based on our own research21–24 ing on environment and modality. Warning calls tend

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 WIREs Cognitive Science Animal communication

Sound source Amplitude Sound attennuation/distortion Receiver

(Sender)

a b
c
A B

FIGURE 1 | A simple model of vocal communication. Sender (A) on the left, vocalizes and the sounds are heard by the receiver (B). Typically,
however, the signal will not arrive in the same state in which it was at the point of departure. Distance alone makes the amplitude of the sound
diminish (called attenuation). Other factors can cause a decrease or even a distortion: ‘a’ signifies another sound source of a similar frequency which
makes it more difficult to perceive the signal sent from A past point a; ‘b’ represents a typical range of possible obstructions, such as trees and shrubs,
refracting the sound; ‘c’ is an often invisible obstruction, such as sounds created by wind, updrafts, and fog, able to distort sounds. At the very least,
B will receive a signal of lower amplitude than at which the signal was sent. In other words, noise and distortions can become a real problem for
communication.

to be swift, while an odiferous message may take a benefit the sender. The problem was that this did not
long time to discover. Such variations in delay time lead to clarity because not all signals benefit the sender
from sending the signal to changing the behavior of the and not even all signals require a change in the recip-
receiver and the intensity of the signal (from obvious ient’s behavior. Maynard Smith and Harper added in
to very subtle) mean that any definition of communi- 1995 that a signal increases the fitness of an individual
cation has to be quite broad. Animal communication by altering the behavior of other organisms detect-
may have evolved specifically to benefit a conspecific ing it, and that the signal has characteristics that have
receiver and, it can be a very efficient way of avoid- evolved because they have such an effect.30–33
ing serious conflict. It may also be possible to argue While this is a useful and widely accepted def-
that animal communication has become more com- inition it is not one that is interested in communica-
plex and cognitively demanding in those instances in tion per se but specifically in signals. Information and
which innovations, sociality, and longer life spans fos- communication do not feature in their accounts. If we
tered the evolution of larger brains and the need for turn to the father of modern information theory, we
more complex communication (Figure 2). are, in a way, no wiser. Shannon devised a number of
So far the passage of a signal from A to B theorems now used in modern radio engineering. His
would be regarded as successful communication if B most famous theorem C = B log2 (1 + S/N) addresses
changed its behavior in response to the signal. The problems of communication. Notably, however, ‘com-
word ‘communication’ is and remains thorny and even munication’ in the mathematical, engineering sense for
controversial at some juncture because implied in it sound transmission is not concerned with meaning
may be an assumption that communication means and contents but with the ultimate carrying capac-
conveying information, when ‘information’ is under- ity of band-limited communication channels, thus far
stood in the sense of ‘meaning’. Others argue instead removed from cognitive science. Indeed, psychology
that such presumption of implied meaning is merely relegated the theory to the realm of statistics and math-
speculative and we should concentrate on measur- ematical probabilities.36
able signals. Thus, the term ‘communication’ itself has Information as it is used in the context of
roused scholars to controversies, also very recently.25 evolutionary biology, ethology, neurobiology, and
Although there are many disparate fields that have philosophy carries first and foremost meaning. Mean-
influenced or shaped animal communication including ing in communication has been extensively explored
mathematics, philosophy, and linguistics,26–29 the real in human language. Whether we go with Millikan’s
controversy and oppositional stance is between those notion of biologically cooperating mechanisms or
who followed Dawkins and Krebs and, later, May- use the original linguistic concepts developed by
nard Smith’s notion of animal signals30–33 and those Grice37–39 about human communication it does not
who insist that information (as content with mean- carry us far in animal communication because the bar
ing) is central to animal communication studies.34,35 is set too high in the sense that humans are said to
Dawkins and Krebs offered a succinct definition, derive meaning from an awareness of each other’s state
namely, that animal signals are actions or structures of mind and they can express such an awareness in
that change another organism’s behavior and thereby language (Box 1).

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FIGURE 2 | Settling of boarder dispute by negotiation and vocal signal. Australian magpies, Gymnorhina tibicen, are territorial birds and use a
ritualized caroling call, sometimes in duet with their lifelong partner, to indicate permanent occupancy. At close range, ritualized signals and
vocalizations can be a very energy-efficient way of solving a conflict without anyone getting hurt. The territorial boarder is clearly marked on the
image. In the upper image two neighbouring magpie groups meet on the ground. Instead of fighting, the two magpie males (A and B), lower image,
approached each other from either side of the boarder. Both then paraded in a slow and deliberate way up and down that stretch of boarder. Then
they stopped and aligned with each other, both caroling. The female of group A (Aa) then crossed the boarder, thought to be an appeasement
gesture, and aligned herself in opposite direction with the other female (Bb). These two are adult females of the respective group and long
established breeding pairs. Once the two females had lined up, they too began caroling with each other. In a second round of caroling, A started,
followed by Aa, then B, followed by Bb. In other words, the second bout of caroling was a caroling duet of the breeding partners rather than of the
ones facing each other off. After a third bout in the same formation, the caroling birds dispersed and walked back to where they had come from (to
left of the boarder for A and Aa, and right for B and Bb). Later observations showed that the group on the right did not move past that line, nor did
the group on the left. Group B had infringed the boarders but did not do so again. The neighbors had reached a genuine and lasting peace for the
season. (Adapted from Kaplan, see Ref 24.)

BOX 1
abbreviated as ISI (inadvertent social informa-
tion) and PI (public information). Inadvertent
WHAT IS INFORMATION? private information can turn into PI and both
Information theory is the quantitative study ISI and PI can turn into cultural (widespread)
of signal transmission and is largely applied practice. In animal communication, most studies
to information technology and communications are conducted in the first category while we have
engineering. However, the term ‘information’ relatively few examples (but increasing) of the
is a widely used term in everyday language third (intentional signaling). It is this second cate-
and generally denotes the acquisition of knowl- gory that has been largely neglected. Yet cooper-
edge from others or from the environment (i.e., ative species in particular may derive their infor-
nongenetic knowledge) that, as Dachin et al.40 mation from the group specific social context for
argue, includes everything that reduces uncer- which most of the signals are meant.
tainty.
Information falls into several different cat-
egories and it may be important for studies in However, new methodologies and changed atti-
animal communication to distinguish between tudes to animals have made it possible to ask new and
the various categories. (1) Personal information different questions and research designs have similarly
only known to the individual or its group, usually changed (in innovative ways) to address the problem
about physical habitat and resources. (2) Social of ‘meaning’ and cognition in animal communication.
information (personal information can become Research has found that there are ravens that con-
public through various means of communication sole a distressed mate, and South African babblers
or vicarious acquisition either via (a) inadvertent in a cooperative framework, negotiate their future
cues (e.g., locational) or (b) via some measure contributions to the raising of offspring well before
of public performance. (3) Overt signals inten- this is put in practice.41,42 In those cases, there is
tionally communicated in any relevant modality, no doubt that awareness of the state of mind of the
other has to precede the actual behavior. While this is

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 WIREs Cognitive Science Animal communication

cognitively complex, and it may be specific to a group that manipulation of hormone levels can induce
and a lifetime, other much simpler changes occur singing and even alter the song control regions in the
that are adaptive and stable and may require rather brain.47–51
little individual cognitive ability. Those theoreticians Alarm calls, and also mobbing calls, have pre-
who prefer to study animal communication as signals sented researchers with a puzzle though (which may
are skeptical of overinterpretations and inferring too also explain the long-standing research in this area)
much from animal signals. The risk for cognitive ethol- since they may not just indicate the presence of a
ogy on the other hand is to underestimate the simple predator but signify a multitude of other things, such
process and the importance of associative learning, be as an attempt by an individual to muster support from
this from cues in the environment or from conspecifics. conspecifics or even from heterospecifics.52,53 They
It remains the most important dictum in science to be may be issued to not only alert others to the pres-
as parsimonious as possible, perhaps especially so in ence of a predator but also draw the predator’s atten-
the interpretation of behavior.43 tion to the signaler, i.e., the calling may be interpreted
It is thus also important to be methodologically as a behavior that is at once life preserving, selfish,
aware that signal characteristics may be learnt or not, altruistic,54 or seemingly suicidal by drawing attention
or intentional (as is implied by the notion of ‘sending a to itself and increasing the risk of capture.
signal’). Indeed, deciphering signaling between parties There have been many explanations that may
(knowing or not) is part of the fascination in many hold in specific situations, one being the ‘pursuit
of today’s research efforts. It also depends where the deterrent’ hypothesis that argues that the calls may
emphasis is placed: (1) on the signaler, (2) on the deter predators from further pursuit because they
means of achieving specific signals, (3) on the nature signal the fitness of the prey.55,56 In such cases, the
and type of signal, or (4) on the receiver. The possible calls are thought to be directed not toward conspecifics
juxtapositions are numerous. but to the predator. In some visual displays, usually
toward ambush predators (such as felines and some
birds of prey), open presence, sometimes accompanied
VOCAL BEHAVIOR by displays of physical prowess in some ungulates,
Among the many forms of vocal behavior (from single called ‘stotting’, is now a well-recognized method
elements to syllables to ornate song), almost all of by some prey species to let a predator know that
which have been studied extensively, alarm calls have their surprise attack has been foiled by discovery and
proven to be particularly useful to study precisely that the fitness and alertness of the intended target
because alarm calls/mobbing calls or warning calls would make capture unlikely.57,58 A further function
are typically short, can be easily measured in terms identified as beneficial for the prey is alarm calling
of origin, use, and response, and because they may for the purpose of changing the behavior of offspring;
also be fueled by either the motivational or intentional silencing nestlings, or making juvenile ungulates freeze
systems. Tinbergen44 recognized four motivational and hide until the mother indicates by calling that the
states: hunger, aggression, sex, and fear. Alarm calls danger is gone, can save lives.59
may fall into at least one or two of these motivational Many contextually specific uses of alarm calls
states (fear and aggression). They may be intentional have been identified (see also recent review60 ). They
(more of this below) in the sense at least that they are may be used for brood training and protection,
implicitly a mechanism for providing a warning of a as has been described in the moustached warbler
specific risk as perceived by the caller to others, hence showing that survival rates increased when a strong
ab ovo involving at least a dyad if not more (signalers positive correlation existed between a parent issu-
or receivers). ing antipredator alarm calls and a chick’s ability
Research has also identified how interaction to perform appropriate antipredator responses.61
with the environment or certain physiological events Alarm calls have been described as an investment in
can alter signals or outcomes. For instance, there is mates62 and as anticipation in future reciprocity.63
substantial variation in an individual’s vocal perfor- The hypothesis proposed by Ridley et al.64 is recipro-
mance, and many of these variables have been well cal altruism, suggesting that mutual protection of the
researched in avian species. Photoperiod,45 change group, while appearing altruistic at the time, will ulti-
of season,46 overall health, genetic endowment, sex, mately benefit the survival of group members. Krams
and age are just some of the variables that affect et al.65 drew similar conclusions in pied flycatchers.
performance and expression of vocal repertoire, and, That song in songbirds is learned in an over-
more importantly, may also reveal certain quali- whelming number of species is no longer a matter for
ties and traits to the receiver. It has been shown debate, after nearly 100 years of research in this field.

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It is extremely well documented in zebra finches,66 in case of this being an alarm call instead of warning
in white-crowned sparrows,67 and in nightingales68 that there is a predator about, the call would specify
and in several other songbirds. In the psittacine group which species type (snake, bird of prey, or feline). It
(parrots, cockatoos),69 corvids (ravens), and the crac- is or can be intentional, in that it is other-directed
ticidae (including Australian magpies), studies have and refers to very specific things that the signaler has
shown that against predictions many of the short observed and passes in the signal.74 Following the
vocalizations, i.e., utterances other than song, are work by Cheney and Seyfarth in the 1980s,75 studies
learnt behaviors70 and that alarm calls are referential of ground-dwelling mammals—including squirrels,
and stable signals.71 Many birds that are capable of meerkats, marmots, and Diana monkeys76–79 —have
lifelong learning (i.e., having a plastic brain) and can shown animals to have a demonstrated ability to
acquire new vocalizations tend to live in cooperative discriminate between different dangerous species and
family groups and may need such versatility for com- produce alarm calls that can even identify the type of
plex social interactions. Such abilities may derive from predator in the call itself.
a high-capacity memory system documented largely in There is probably not a single extant avian
songbirds and primates.72 species without some means of issuing an alarm call.
Yet most documented examples of teaching and To do so referentially, however, could not be assumed
skill acquisition in animals, and these are surprisingly because it could simply derive from affect (i.e., reflect
scant as a recent review found,73 are not related to a motivational state). To ascertain this, such calls
communication but to the business of living in gen- had to be tested experimentally. In quite a few cases
eral. For instance, teaching offspring has been found in of disparate avian species, for instance, as in chick-
relation to hunting skills (ranging from otters to lions ens, in bobwhite quail Colinus virginianus, ravens
and eagles), then, in much smaller measure, to forag- Corvus corax, yellow warblers Dendroica petechima,
ing skills, motor skills, food, and/or predator identifi- black-capped chickadees Poecile atricapilla,80–84 and
cation. Only a very small number of publications on Australian magpies Gymnorhina tibicen64 referential
active teaching of offspring are related to skills specif- alarm calls were found. That is, it was clearly shown
ically related to communication.73 We cannot tell at that the species in question referred to an identifiable
this point whether this distribution of skill attainment external stimulus (as compared to its own motiva-
by active teaching reflects actual practice or is the tional state). Referential signals so far discovered and
result of researcher bias. Teaching itself requires some studied include both alarm calls and food calls, be this
form of communication and performance by the recip- in primates or in birds.
ient. It is fair to say that the rush to identify signals in In 2007, Evans and Evans85 made an important
all its possible variations has led to a certain neglect distinction between referential and representational
of developmental aspects. It also seems that there is calls. In a controlled set of experiments the researchers
a tendency to assume that learning largely occurs as established that referential and representational calls
observational and associative learning rather than via may not have the same visible impact on the receivers
active teaching. Yet some avian species and some pri- of the call. In referential signals, particularly in alarm
mates have an exceptional long period of development calls, there is an immediate response by the receiver.
and spend considerable time growing up in their natal In representational calls responses may not always
or family group, surrounded by group members or be forthcoming. Representational calls, such as a
at least accompanied by one parent. In the latter sce- food call, may relay the correct message of food
nario, it is not far-fetched to postulate that acquisition availability86,87 and even be specific as to quality
of communicative skills is favored in social species. and amount88 but, as Evans and Evans85 found, the
recipients responded when they had not fed but did
not respond if they had recently fed. Hence, the
REFERENTIAL SIGNALS signal may well have been heard and understood
The idea of motivational versus intentional signals but not always acted upon. This means that the
has been raised repeatedly. The former refers to an recipient’s understanding of that signal may well
internal event, the latter to an actual external event. remain unobservable. In terms of definitions of animal
Connected with it is the need for an individual to communication as signals that require a change of
indicate clearly what it is that is to be imparted to a behavior in the receiver, the discovery undermined one
conspecific. A referential signal is a stable and univer- of these key definitional pillars. Moreover, not acting
sally understood signal (at least by conspecifics in a may also involve active decision making.
regional context if not further afield) that has a seman- In summary then, there are multiple possibili-
tic content rather than being generalist. For instance, ties of what recipients will and can take from signals.

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Hence, the basic definitional condition that a message development.97 Not surprisingly, gestures have been
needs to show a change of behavior in the recipient studied extensively in primates.
simply does not and cannot describe all forms of inter- Until very recently, there was no expectation
action when, arguably, communication has occurred. that referential gestures would be possible in species
By contrast, the ‘message’ in the alarm call may other than primates, because it was thought that
not just contain a general warning that a predator hands and arms were needed to engage in pointing
has been spotted but the recipient may also decode and gestures. Recent research by Kaplan98 has found,
from it the predator’s size,88 the urgency or nearness however, that the Australian magpie G. tibicen is able
of danger,89 or even something about kinship, sta- to point referentially, as shown in a series of controlled
tus, age, status, and sex of the caller.90 Recipients experiments in the field using a taxidermic model
may vary their responses accordingly. For instance, of a wedge-tailed eagle Aquila audax, one of their
in Californian ground squirrels at least, information predators.98 The first magpie, on discovering the eagle,
about age of caller prompts a different response in vocalized and used its beak to point at this half hidden
listeners.91 Alarm calls by juvenile vervet monkeys eagle placed under a small tree. The subsequently
tend to get ignored because they are unreliable and arriving magpies then watched the pointing of the
at times incorrect but the same vervet monkey juve- first bird, followed its direction, and then also pointed
niles may learn to recognize the alarm calls issued by until the entire group was present. The pointing
starlings.92 gesture was not carried out so that the magpies could
The fact that animals may recognize signals of get something for themselves (as in gestures used in
heterospecifics and act on them is intriguing because, begging for food), but to let the remainder of the
in those cases in which alarm calls are clearly not part group know of the presence of the eagle. The posture
of a species’ genetic makeup, their recognition has to was exaggerated and differed markedly from other
include some form of learning. Recognition, in this postures.97 Referential pointing has now also been
case, has to include its specific representational value shown in ravens.99 Australian magpies are a social
of a real event or a potential danger (warning of a species, as are common ravens and primates, and their
predator). There has often been a nagging question survival hinges on cooperation which may foster the
whether certain similarities of a heterospecific signal evolution of complex signals. Cooperation and group
may not be enough to trigger the same response as living may thus be important variables to consider in
the one used by a specific species.93 However, when the study of communication. Indeed, Bouchet et al.100
a starling utters a referential alarm call, the charac- found, when comparing some primate species, that
teristics of the bird calls are substantially different social complexity parallels vocal complexity.
from the sound characteristics of any vervet monkey
vocalizations. If they have rather little in common why
should a starling’s alarm call trigger an appropriate THEORETICAL DEVELOPMENTS
response in a vervet monkey? Sound properties are an Researchers in the 1950s and 1960s were obviously
unlikely source of such a response. Hence, acquisition fully aware of the risks of overtheorizing the behav-
of knowledge by experience and based on a set of ior of animals and instead opted to simply record
specific and reliable cues may teach a monkey to heed and document what they saw and heard. They tended
the bird’s call each time. The starling’s call has thus to categorize calls and visual displays and placed the
meaning.94 emphasis on the sender and on specific functions, most
Referentiality is not confined to auditory expres- of which had to do with basic survival tasks, such
sion although they are the only ones capable of being as actions concerned with reproduction, food, preda-
expressed across substantial distances. Visual signals tors, territory, or offspring. Signals were not labeled
tend to be at close range, within sight of the receiver. as such, instead authors described behavior as display
Claims that they may be semantic or functionally behavior or vocal behavior and thus avoided many of
referential have usually not been made. Indeed, visual the pitfalls of communication theories while providing
signals, apart from those associated with mating, have a wealth of knowledge. They did so in such engag-
all too often tended to be ignored and yet they often ing ways of writing and provided meticulous details
play a significant role in the communication of ani- that the accounts of displays and other behaviors are
mals. Gestures in apes and other primates, however, still important and a pleasure to read today.17,101,102
are a very important exception18,95,96 because ges- Specifically, they left behind a detailed record of ritual-
tures are processed in the equivalent area of the brain ized behavior, such as greeting and courtship displays
as speech in humans and hence these visual signals offering invaluable and never repeated insights into
have been seen as putative precursors to language the daily lives of birds and other animals.

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Ritualized behavior, no matter how complex, high-pitched chirps in the same circumstance. A
may consist of one simple and unambiguous mes- chutter-like call is made for a snake and a single
sage. Males may advertise themselves as outstanding cough-like call for an eagle. Seyfarth and Cheney106
breeding candidates or the display may say ‘stay found that, when the call they had identified as indi-
away’ when territorial boundaries need defending. cating the presence of a leopard was played back, the
Courtship rituals, by contrast, rely on careful mutual monkeys would dash to the nearest tree and climb
attention of two players who need to coordinate it. On hearing the snake call, they would stand up
their activities rather precisely if an agreement for a on their hind limbs and peer into the grass. When
union is to be forged. One of the best known and the eagle call was played, they would look up and
most dramatic courtship rituals that seals a lifelong take cover. Some years later, as already mentioned, it
bond and largely relies on motion and body posture was found that chickens make different calls for aerial
is performed by grebes (Podiceps ssp.) as a dance on predators than they do for predators on the ground.74
water. In horned grebes Podiceps auritus, the male The researchers played back to hens the recorded calls
‘bounces’ forward, dives several times, then both made by the cockerel in response to seeing a ground
male and female rise to full height by treading water, and an aerial predator in a controlled setting, i.e., a
facing each other in what is sometimes referred to as cage in the laboratory. Here the hens could not see any
a ‘penguin’ display; they continue to dance in that predators and were not exposed to any other stimuli
posture until finally swimming apart. Lyrebird males that might cause them to vocalize. They tested each
(Menuridae sp.) are famous for their dancing as well female chicken individually playing the two kinds of
as for their vocal displays in courtship dances.103,104 alarm signals through a loudspeaker. When the aerial
The most exceptional and unique display is one per- alarm call was played, a chicken hearing it crouched
formed by the Albert lyrebird and was first described and looked up as if trying to catch sight of the preda-
by Curtis103,104 but went largely unnoticed by the tor in the air. When the ground-predator alarm call
world. The male displays on a mound in the depth of was played, the chicken hearing it ran for cover or
forests of Eastern Australia and dances, revealing a strutted while calling in a way that might drive the
specialized set of feathers (the lyre) that is shimmered predator away. Thus, the two alarm calls have speci-
during the dance. While he dances he also sings in the ficity and signal to the receiver to take the appropriate
loudest and most melodious pure tones of any bird measures to avoid being caught. In both cases, be it
known. Most of the sequences of song are mimicked vervet monkey or domestic chicken, it was shown that
snippets from other birds, cleverly choreographed two species, far removed phylogenetically from each
(with transitional segments, lead-ins, and fade outs of other, had developed signals that were functionally ref-
an accomplished musician), and delivered forcefully. erential. They further tested and were able to show
However, the piece of the display that is most astound- that these calls were produced intentionally.
ing is the male’s ability to add yet another dimension The operational definition for intentionality was
to the performance, namely percussion. With his left rather simple and ingenious. To be regarded as an
foot, he holds on to a vine that typically grows to full intentional signal, the caller needed to make the call
height of trees particularly in wet rain forests. Then only when it had an audience. That is, even when
he pulls on the vine and does so rhythmically, fitting seeing the predators, no calls should be issued if
with his song and dance, a movement that generates there was no audience. Indeed, this was the case.80–84
a clearly audible rustling and swishing and becomes a Hence, the interpretation that animals just act in affect
percussionist addition to the performance. Why this and cannot help themselves but utter emotive calls was
is remarkable is that animals have been consistently disproven.
thought of as being incapable of producing rhythm, a By having shown the various segments that
trait thought to be unique to humans.105 make for unmistakable acts of communication, the
Most of the papers on displays remained descrip- groundwork was laid for claiming and investigating
tive and, while fascinating, were not designed for communication in animals in which both the signaler
formulations of theories of communication. In the and the receiver (or reactor) understand the context
1980s, however, a major shift in thinking about and and can act accordingly.
researching into animal behavior is usually attributed Intentionality has been a topic of great interest
to a paper reporting the very specific meaning of in philosophy for centuries partly because it seems to
alarm calls of vervet monkeys showing that adults attest to freedom of choice and thought. In science,
had different calls for various predators call.106 Male by contrast, preference was at first given to think-
vervet monkeys, Cercopithecus aethiops, make a deep ing of such acts, even if intentional, as adaptive, i.e.,
barking call for a leopard and females make short, as part of a template and genetically fixed. Seyfarth

668 © 2014 John Wiley & Sons, Ltd. Volume 5, November/December 2014
 WIREs Cognitive Science Animal communication

and Cheney,107 however, also dispelled this notion by a preinstalled game. Actor and reactor were playing
showing that juvenile vervet monkeys made mistakes out the same game of self-preservation. The model
when practising their own version of issuing warning was built on conflict and competition and sported a
calls. In other words, it became clear that this behavior vocabulary and considered scenarios deeply indebted
had to be learned, involved recognition of the ani- to capitalism. The vocabulary is the same and the
mals that are dangerous (despite similar silhouettes, goals are the same. Everyone is in it to win and will
neither a vulture nor a stork but only an eagle is dan- fight for dominance, driven by a basic instinct, or
gerous), and clearly involved memory of predators, rather by genes programmed to reproduce themselves.
attributing the correct call to each and making a call In this concept, altruism was logically impossible and
only when others were present to be warned. Learning cooperation was seen as a means to a selfish end
and cognition were involved and this set the scene at best.110,111 Dawkins produced the logically most
for an entirely different and new line of investigations coherent, if not brilliant, communication theory ever
about animal behavior in general and animal commu- considered but it was deeply pessimistic if not cynical
nication in particular. It also became clear that such and ultimately also flawed. Indeed, it seemed that cog-
investigations would benefit greatly from some degree nition had disappeared entirely and was almost super-
of interdisciplinarity and indeed the field of animal fluous and itself suspect of human overinterpretation.
communication has interacted with and mutually ben- Decision making as an act representing choices had all
efited from neuroscience, specifically neurophysiology, but disappeared and developmental studies were out
and neuroethology, comparative psychology, ethology, of favor.
ecology, even musicology, and developmental biology What followed was the application of game
and acoustics. theory to animal interactions which, as has recently
However, at the same time as these discoveries been argued, has played a major role in reshaping our
were made, the theory proposed by Wilson108 in 1975 view of animal communication, transforming it from
was powerful enough to almost halt progress in the a mutualistic sharing of information into a self-serving
cognitive line of investigations (except in primatology) contest between ‘mind readers’ and ‘manipulators’.112
for another two decades. Wilson said that communi- However, true to the characteristics of selfishness,
cation is an action by one organism that alters the human imagination soon discovered that selfish-
behavior pattern of another organism in a fashion that ness, as manifested in signals, can include deception,
is adaptive to either one or both of the participants. manipulation, and coercion to name a few key fea-
The word ‘adaptive’ is important here. Wilson said tures, qualities that can be adaptive, as in plants and
that by ‘adaptive’ he meant that the signaling, or the some animals, but they can also be based on cognitive
response, or both, have been genetically programmed processes, decision making, and experience.113,114
by natural selection.108 Hence, this definition confines In so doing, cognition came back in by the back-
communication to events (for signaler and receiver) door into various theories, such as theory of mind
that have become part of the genetic characteristics of applied to great ape research projects and finding its
the species. Means of communication that are learnt most fascinating expression in a book by Whiten and
during the individual’s lifetime, and may be passed on Byrne115 called Machiavellian Intelligence. Indeed,
from one generation to the next by cultural transmis- deception has been documented in species other than
sion, are not included in Wilson’s definition of com- primates. Møller, for instance, showed deception in
munication. Of course, genes always play some role status signaling in house sparrows, Passer domesti-
in behavior—for example, genes determine whether cus,116 and false alarm calls for the purpose of resource
we have hands or wings and such factors influence usurpation in domestic chicken,117 in great tits, Parus
what kinds of signals can be sent. But that is not major,118,119 and similarly in drongos, Dicrurus par-
what Wilson meant by adaptive signaling; he meant adiseus that managed to trick mixed-species bird
that the behavior of signaling, or the behavior of the flocks for resource usurpation.118,119 These observa-
response itself, is to a large extent controlled by genes. tions about false signaling have sneaked into accounts
The book by Dawkins109 followed just a year after in such a way that the cognitive complexity cannot be
Wilson’s but while following closely in Wilson’s foot- denied. However, even in deception it is not always
steps it radicalized the theoretical perspective of the achieved by false alarms or calls. For instance, some-
drivers for behavior. For Dawkins, behavior was only thing I observed in South America, a capuchin male
a by-product of the actions of the genes. Accordingly, discovered a rich food source in fallen fruit. He was
all that needed to be established was whether an action alone. He saw it, turned around, and when no-one
had benefits or costs. The advantage of this perspec- was looking he gorged himself on the fruit, making
tive was that all life was interconnected by playing no sound whatsoever. Then he took fruit in his hands,

Volume 5, November/December 2014 © 2014 John Wiley & Sons, Ltd. 669
 Advanced Review wires.wiley.com/cogsci

as many as he could carry, hid under a tree, and con- explained why birds can mimic sounds not part of
tinued feeding rapidly. He then dropped the last bit of their own species repertoire (and thus not part of its
fruit, walked on and away from the scene, waited, then own genetic template).
turned around, and gave a food signal. Others joined In addition, technology concerned with commu-
him soon after and the group was feeding together. In nication and with acoustics has moved so far ahead
other words, the food signal was ‘honest’ but he had that we can measure accurately just about any sound
simply delayed it to ensure that he had his fill first. from infrasound to ultrasound and anything in the
While coercion and aggression may not demand any visual spectrum. Acoustic specialists have pushed the
cognitive capacity, deception and manipulation do. science of sound to new heights and neuroscience
The more intelligent an organism is, the more devious now has sophisticated neuroimaging. Here methods
it can also become. There may be punishments and have become very important. Researchers, such as
corrections if found out120,121 but such signaling is Suthers, have perfected techniques to test vocal pro-
clearly rule-breaking and designed to deceive. It must duction in living birds130 and Marzluff was perhaps
be based on a decision that the individual made. the first to show how a supposedly esoteric topic
like face recognition in corvids and concomitant brain
activity could be demonstrated in a living bird using
NEW EVIDENCE: NEW DIRECTIONS? neuroimaging.128,131 Moreover, mirror neurons have
The most recent theoretical development that has implications not just for imitation, learning, and mem-
had, and no doubt will continue to have, a crucial ory formation but also for intentionality. Iacoboni
impact on many fields but especially on cognition and et al. went so far as to entitle one of their papers
communication comes from the astounding findings ‘Grasping the intentions of others with one’s own mir-
in neuroscience. In 2009, Rendall et al.122 were still ror neuron system’.128
able to argue that animals may only appear as if Also new are research designs that investigate
they understand (for instance a semantic contents of the ability in human actors to select communicative
vocalizations) but that it was virtually impossible to actions, i.e., actions directly designed to modify the
prove this (for review, see also Ref 123) and hence, mental state of another agent without using language
by implication, it was beyond scientific inquiry. That or traditional communicative channels. Studies by
impasse is increasingly broken via the progress that is Galantucci132 or Noordzij et al.133 demonstrate that
being made in neuroscience, following behavior while neural correlates of intentional communication can be
simultaneously tracking brain activity, eye movement, shown to exist by using a simple movement of geomet-
or vocal tract activities. First, the mapping of the ric shapes that the sender knows but the receiver does
song control system in birds,124,125 followed by the not, forcing the sender to find ways of communicating
identification of a speech-related center (used for without words. By using an event-related functional
gestures) in monkeys and apes,126,127 told us precisely magnetic resonance imaging design, they were able to
about the relationship between specific signals and isolate cerebral activity evoked when planning a com-
brain activity. In the case of birds, this research has municative action and when interpreting the meaning
identified where, how, and what learning occurs in of that action. As Noordzij et al. show, and I quote:
the acquisition of song and the capacity for long-term ‘These cerebral responses, in both sender and receiver,
memory of vocal signals. were localized in the right posterior superior tempo-
Indeed, between 2004 and 2008 the cognitive ral sulcus (pSTS), a region previously associated with
field of avian and primate studies advanced in such attribution of intention and they were independent
fundamental ways that it is almost impossible to con- from sensory inputs and motor outputs’.132,133
ceive of how we thought before these discoveries were It has been legitimate to remain skeptical when
made. First, mirror neurons in macaques were discov- assumed cognitive processes could only be inferred
ered and described in a series of papers by a team in and the results at risk of being overinterpreted. How-
Parma, Italy, showing that movement can be learned ever, neuroscience has become instrumental in putting
by encoding movement of others in the observer’s the arguments about the absence or presence of cog-
brain and then imitated against this representation.128 nitive processes from inference of observed behavior
In 2008, Prather et al.129 discovered that there are squarely back into biology by producing evidence of
mirror neurons for vocalizations in birds, used for highly specific forebrain activity. Such methods seem
learning and learned vocal communication. They to offer great potential for future research in animal
showed convincingly that a bird listening to a conspe- communication. Brumm134 argues that many special-
cific’s vocalization activates neurons that would also izations have come together or overlap to have pro-
fire had the bird sung the same passages itself. It also duced the achievements so far.

670 © 2014 John Wiley & Sons, Ltd. Volume 5, November/December 2014
 WIREs Cognitive Science Animal communication

FIGURE 3 | Diagram describing the process of signal transfer. A sender may see a predator (visual experience), the image is processed in the
brain (representational integration or dissociation). The image is recognized (memory) and identified as representing danger—then this bundled
information, consisting of the visual image just seen plus the interpretation of it drawn from memory (be it acquired by experience or learning), is
followed by a translation into a different modality, as a vocal signal—heard by receiver—and in this case there are even more processes involved
because it may involve assessment of quality of signal, origin of caller, seriousness of event, location, and urgency plus judging the auditory signal
across space taking into account attenuation and possible distortion; then the receiver translates the auditory signal received into a
representational/visual concept and on this basis makes a decision on whether or how to act in response.

THE FUTURE: CONCLUDING the Wulst, and the amygdala? How does cross-modal
REMARKS integration work in animals,135 is there a hierarchy
in which stimuli are processed? Does an organism
Neuroethologist and ornithologist have been hand in respond faster if it is in one modality or another? How
glove for decades of research on song and prima- does the initial assessment by the animal come about?
tologists have worked on cognition of apes together
And in which region(s) of the brain is it processed? For
with neuroscientists and psychologists to identify
instance, we discovered in free-living Australian mag-
precise areas of the brain involved in gestures used
pies (only the second avian species tested in the natural
to communicate. How differentiated are the visual
environment) that assessment as opposed to attack of
and vocal/auditory pathways used in communica-
a predator is processed in different hemispheres.136
tion and what kind of processing takes place and in
which hemisphere of the brain? In human infants, for Magpies used the left eye/right hemisphere (LE/RH)
instance, sensory pathways are relatively undifferen- prior to withdrawal and the right eye/left hemisphere
tiated and lead to cross-modal influences in infants’ (RE/LH) prior to an approach. Viewing prior to
perception.132,133 approach was low arousal (alert posture not adopted)
Signals in the environment are rarely mono- and withdrawal of high arousal. Withdrawal is there-
modal but multimodal. Important to add here is that fore a behavior that results from processing visual
even a signal in one modality (say a visual signal) usu- information in the RH (receiving inputs from the
ally cross-cuts modalities in a single organism in the LE), whereas approach follows processing by the LH
sense that objects perceived visually are translated into (inputs from RE). The RH appears to control most
auditory signals (Figure 3). How do these translations aspects of predator–prey interactions, suggesting that
from visual to auditory and back to visual work? Are a suite of antipredator strategies may have been orga-
there specialized mechanisms or is this reliant on gen- nized within the RH.137 But we do not know whether
eral cognitive capacity that involves the integration at signals about predator–prey interaction are therefore
many levels in the brain including the hippocampus, also largely processed by the RH.

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 Advanced Review wires.wiley.com/cogsci

Cognitive scientists distinguish between several There is an international society for the study of
core knowledge systems, such as those related to attention and performance.144 While their interest is
physics, mathematics, geometry, and psychology. The in the human species, every single part of their work
debate is very well summarized in a recent review by would be important to investigate in animals and be
Vallortigara et al.138 It also suggests that signals could very interesting in the study of animal communication.
be investigated in terms of the knowledge systems we First of all, a very basic concept that seems to get lost at
already know are well developed in birds and primates times is that communication is dynamic and it is a pro-
and even in some invertebrates so far tested. cess. It derives from one living organism with a certain
That the research in the field of animal commu- age, ability, life experience, and individual confidence
nication has entered a new phase is obvious in the to identify something in the environment worth telling
many recent and vigorous debates. They are not all others about or even advertising or getting frightened
going in the same direction. Sociobiologists continue by—be this triggered by a food discovery, territorial
to assert, although at a very sophisticated level (and incursion, a predator, an irregularity, or a novel object
having left the backdoor open for cultural transmis- and it may require translation from one modality into
sion via ‘memes’), that genes determine everything and another (Figure 3). We know far too little of the brain
at the other end of the spectrum are those who think mechanisms underlying cognitive processes in making
animals are capable of free thought. Others argue that and receiving signals and should be emphasizing ques-
there is too much anthropocentric interpretation. By tions of why, what, and when information from the
using the words ‘information’ and ‘meaning’ when environment is processed; also whether there are sub-
describing signals, we have borrowed terminology stantial species differences and what these are.
from linguistics that may be misleading and a dis- For example, a recent review of functionally
service to science.122 Animals are said to respond referent signals145 reminded us that signals may be
to underlying acoustic structures and that, so signal intrinsic (internal events of caller) or extrinsic (con-
research argues, are what we should look at.123 In a cerning something in the environment) and that we
recent review of referential communication in mam- have evidence of referential signaling of far too few
mals, it was admitted that we do not know enough species. That is true but how will the next ones be
(actually: next to nothing) on how animals categorize chosen and for what good theoretical reason? It would
their environment.139 Such categorizations are per- appear to be very fruitful to test species known to be
ceptual and suggest that varying sensory dimensions cooperative group living animals and long-lived. It is
are continuously transformed into symbolic equiv- noticeable that avian species that have been chosen
alence classes for producing reliable behavior.64,140 tend to be natives of the Northern Hemisphere. How-
How varying acoustic structures are perceived and ever, most of the cooperative and long-lived avian
categorized might therefore provide crucial insight species are natives of the Tropics and the Southern
into the cognitive domains of animals and there is no Hemisphere and the underrepresentation of such
reason to presume that they are the same categories species in any debate (even when there are research
that humans have made for themselves. publications of such species already available) has
Importantly, there are also questions about a limited the opportunities to test hypotheses of signal
relationship between sociality and signal complexity, characteristics against parameters of life history (and
and between long periods of maturation and cogni- high brain to body weight ratios). To date, we have no
tive ability. The point has recently been made that evidence as to whether signal characteristics alter or
long-lived species are more likely to be social, or multiply in number or get more into the multimodal
rather, from an evolutionary point, that group living range or become even more subtle with sociality.
fosters longer term survival.64,140 It is not just affect but reliable and possibly even
Group living with horizontal and vertical hier- more precise signaling that may be important, as
archies have been said to constitute the preconditions diversification of signals might imply.
for complex communication and higher cognition. The field is wide open and it would appear to be
These capabilities have been associated with and premature to pit effect of signals against ‘information’
explored in communication among great apes, dogs, or to suggest that the framework for functionally
wolves, and dolphins.141–143 Only in recent years has referential signals has been either so undermined or
a link been made between these social variables and exploded146 that we can drop it as a useful term. In
the expression of complex cognitive abilities in the fact, a new chapter has just started and it is largely
vocal behavior of mammals and avian species.25 unexplored.

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 WIREs Cognitive Science Animal communication

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FURTHER READING
Bradbury JW, Vehrencamp SL. Principles of Animal Communication. 2nd ed. Sunderland, MA: Sinauer Association US;
2011.
Rosenqvist G, Admundsen T, Esprnark Y, eds. Animal Signals: Signalling and Signal Design in Animal Communication.
Trondheim: Tapir Akademika Publishing Press; 2000.
Searcy WA, Nowicki S. The Evolution of Animal Communication: Reliability and Deception in Signaling System. Princeton,
NJ/Oxford: Princeton University Press; 2005.
Wyatt TD. Pheromones and Animal Behavior: Chemical Signals and Signatures. 2nd ed. Cambridge: Cambridge University
Press; 2014.

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