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their prominence can be hard for even signals or any other behavior. Together,
Primer a casual observer to overlook. Animal these three scientists emphasized the
signals therefore raise many scientific importance of entering the perceptual
questions: What are their functions? world of animals to fully analyze and
Animal signals What information do they transmit? understand animal signals. Their work
How are they produced? And why did underlies much of the current scientific
Mark E. Laidre1 they evolve? research on animal signals.
and Rufus A. Johnstone2 Pioneering empirical work on
animal signals was carried out by Subtleties of animal signals
The study of animal signals began Karl von Frisch, Konrad Lorenz, and Many animal signals may ‘jump out’
in earnest with the publication Niko Tinbergen, three ethologists at the human observer, because
in 1872 of Charles Darwin’s The who were awarded the Nobel Prize they utilize sensory modalities to
Expressions of the Emotions in in 1973. Karl von Frisch decoded the which humans are highly attuned,
Man and Animals, which laid the famous ‘waggle dance’ of honey bees, but other signals can be harder to
basis for a comparative study of showing that seemingly insignificant detect, involving modalities that
signals across all animals, including dancing motions that bees make inside are outside our species’ sensory
humans. Yet even before Darwin, the hive can tell other colony members perception. For instance, electric
the exceptional diversity of animal the precise location of distant food fish utilize discrete pulses of electric
signals has gripped the attention of sources. Lorenz integrated himself into discharge in aquatic environments
natural historians and laymen alike, as the daily activities of geese, allowing to communicate. Given the diverse
these signals represent some of the them to imprint on him, and he thereby channels through which animals
most striking features of the natural identified many of the nuances of their communicate — encompassing
world. Structures such as the long communication. Niko Tinbergen, an chemical, electric, acoustic, optical,
ornamented tail of the peacock, the astute field observer, disentangled and tactile modalities — there are
roaring sounds of howler monkeys, signals that gulls and other animals clearly abundant avenues for signaling,
audible kilometers away, and the use in territorial conflicts. Tinbergen as well as ample biological raw
pheromone trails laid by ants to guide was also responsible for bestowing material that can be co-opted for
their nestmates to resources are each an essential framework for studying signaling functions. This underscores
examples of animal signals (Figure 1). animal signals — his ‘four questions’ an important lesson for researchers:
Indeed, because signals evolved for about the phylogeny, function, not all animal signals are necessarily
the purpose of communicating (Box 1), development and mechanism of prominent, and so acute sensitivity

Figure 1. Diversity of animal signals.

From top left: peacock (Pavo cristatus) displaying its elaborate tail feathers (courtesy of Jessica Yorzinski); wasp (Polistes dominulus) variation
in facial ‘badges of status’ (courtesy of Elizabeth Tibbetts); chimpanzee (Pan troglodytes) gesturing (courtesy of Michael Tomasello); Túngara
frogs (Physalaemus pustulosus) spectrograms of chuck calls (courtesy of Michael Ryan); mandrill (Mandrillus sphinx) colorful red face (courtesy
of Mark Laidre); southwestern speckled rattlesnake (Crotalus mitchellii) with rattle exposed (courtesy of Harry Greene); peacock spider (Maratus
volans) raising its legs and abdomen in display (courtesy of Madeline Girard).
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Box 1.

Defining signals and a framework for their investigation.

Signals can be defined in a four-part definition:

(1) acts or structures produced by signalers, which
(2) evolved for the purpose of conveying information to recipients, such that
(3) the information elicits a response in recipients, and
(4) the response results in fitness consequences that, on average, are positive for both the signaler and the recipient.

For example, when a hermit crab raises its claw, performing a threat signal, it provides information about its intention to attack, which a
recipient can then respond to by fleeing, which ultimately results in both the signaler and the recipient benefiting by avoiding an esca-
lated fight.

Signal Information Response Fitness consequences

Threaten

Signaler’s Recipient ++ +–
intention flees from
to attack signaler – + ––

Each part of the definition of a signal provides a guide to key empirical measurements that must be made to fully understand the signal.
First, the form of a signal must be precisely described and quantified, often requiring specialized equipment (e.g., a spectrometer for
reflected light signals or audio recording equipment for acoustic signals). Second, a consistent correlation must be established between
the use of a signal and the particular contexts (e.g., signaler attributes or environmental parameters) that have relevance to the recipient,
to show that the signal is reliably informative. Third, the probability of the recipient’s behavior changing between different states must be
quantified after (compared to before) it received the signal, to show the signal alters the recipient’s response. And fourth, and perhaps
most difficult, the impact on reproductive success that such signaling interactions entail must be established for both the signaling and
recipient parties, to determine whether each party — as expected — is benefiting on average. Each of these objectives should ideally be
examined both observationally during natural interactions as well as in experimentally controlled situations.

to the perceptual world and the constraints on the efficacy of signal altering group mates to an external
environmental constraints faced transmission, distorting or degrading danger, or begging for food from
by one’s study organisms is vital, the signal as it travels to its target. one’s parents). In all these contexts,
otherwise many of the subtleties of Certain modalities may thus provide a different types of information are
animal signals may be overlooked. superior solution for communicating in conveyed (Box 2), which may at times
a given environment — e.g., acoustic necessitate different forms of signals
Constraints and contexts signals for communicating in dense to accomplish the communicative goal.
Even when signals occur in modalities forests where visual signals would For instance, Darwin pointed out that
familiar to humans, they may still prove be inadequate. The duration of the signals with opposite meanings often
challenging to detect due to selection signal also places constraints on have opposite forms. This ‘principle
pressures that favor subtlety over which modality is optimal: viscous of antithesis’, as he called it, explains
conspicuousness. Signals can thus chemical signals that last for extended why a dog approaching with hostile
vary along a continuum on a variety periods can serve well as long-lasting intentions instead of affectionate
of axes, from ‘conspiratorial whispers’ territorial markers, whereas rapidly intentions exhibits such different
(close-range, understated, and directed fading acoustic calls will serve well signals: the hostile dog is prepared to
to a single recipient) to extremely as alarms that designate momentary attack and so assumes a posture that
prominent signals (broadcast over external threats. Overall, environmental is in accordance with its readiness to
long distances to a large audience of constraints shape the design of signals, aggress, whereas the affectionate dog
recipients). Where a given signal falls especially a signal’s modality and form. does exactly the opposite to guarantee
on this scale will depend on many The social contexts of signaling, its lack of hostility is not mistaken.
factors, including the social context however, also matter, and animal Thus, a signal’s design is also shaped
in which signaling occurs, the chance signals are used in a variety of by the information it must convey.
of unintended eavesdroppers (e.g., contexts, both between different
predators) intercepting the signal and species (e.g., signals used by prey Cues vs. signals and the evolutionary
the environment through which the to deter predators) and within a origins of signals
signal must travel. The environment, species (e.g., signals use for mate An important distinction can be made
for instance, can impose strong attraction, intimidating rivals, between a cue and a signal. Like
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signals, cues can provide information

to others. For instance, the rustling of a Box 2.
mouse as it forages in the undergrowth Some types of information conveyed by animal signals.
is a cue that may convey information to
a predator about the mouse’s location. Internal environment – signaler’s attributes
However, this information is purely a Species, sex, age, group membership, kinship, individual identity
by-product of the mouse’s foraging Location (e.g., direction or distance from recipient)
activity: the rustling was not shaped Condition or quality (e.g., weight, body size, age, health, mating receptivity)
by natural selection to convey that Fighting ability, strength, resource holding potential, or dominance status
information. In contrast, signals have Motivational or affective state, emotions (e.g., fear or hunger), subjective resource
been shaped by natural selection for valuation, willingness to escalate a contest, aggressive intentions, probable future
the specific purpose of conveying actions (e.g., attack)
information and thereby influencing
others’ behavior, ultimately impacting External environment – features of the outer world
both the signaler’s and the recipient’s Referential designation of objects or events (e.g., predator presence or type, danger
fitness. level, or quantity or quality of food sources), either immediately present or remote
in space or time
While cues differ from signals,
many signals may have evolved from
what once were cues. For instance,
a number of species exhibit threat food source is red. When such biases recipient. Dawkins and Krebs went
signals involving prominent postures exist it may then favor the evolution so far as to suggest that the idea of
or bodily movements that indicate an of signaling traits that exploit the bias signals bearing information should be
individual’s aggressive motivation or (e.g., males may develop red coloration abandoned entirely.
fighting ability. These threat signals to attract females for mating). Such The logic of this ‘manipulation
are often abbreviated forms of a sensory exploitation appears to have argument’ was elegantly modeled
species’ natural attack pattern, with occurred in mate choice for many with evolutionary game theory by
individuals exposing their weaponry or species, one example being the John Maynard Smith. Maynard Smith
positioning themselves in preparation chuck call of Túngara frogs, which envisioned a population of animals in
for conflict. Over evolutionary time, is extremely attractive to females, which a certain signal reliably provides
such intention movements appear to even females in species where information to recipients, for instance
have been ritualized into prominent males have never evolved the call. by honestly indicating the likelihood
and highly stereotyped displays, which However, signals that have originated of a signaler attacking. Now consider
can convey the likelihood of an animal through recipient precursors need not the consequences of a mutant that
attacking. As such, animals need not remain entirely uninformative. Recent performed this same signal even
always undertake an all-out escalated evidence in splitfin fish shows that when it did not intend to attack. This
fight, but can potentially use relevant even when signals originate from such dishonest mutant would invade the
signals to make critical assessments ‘sensory traps’ they can later become population, because it could drive
beforehand. In a similar manner, reliable indicators of key aspects of opponents away from precious
Darwin first pointed out that many male quality. resources despite having no intention
vocal signals that animals perform to follow through with its signal.
appear to have originated from altered Signals as information Eventually, the entire population would
breathing patterns that initially may or manipulation exhibit this dishonest signal, making
have been cues, correlated with the Sensory exploitation as an evolutionary the signal worthless and uninformative.
types of physical action the breather source of signals raises a more general The problem of dishonest mutants
was preparing to undertake. question: are signals fundamentally seemed intractable until Amotz
The evolutionary process by which informative (providing the recipient with Zahavi suggested a solution: the
signals evolve from cues is known useful information that helps it choose ‘handicap principle’. The handicap
as the ‘signaler precursor route’. the right response) or are they instead principle suggested that some
In this case, the signals originate manipulative (deceiving the recipient signals might be too costly for a
from behaviors or structures that by inducing a response that is good signaler to fake. For instance, certain
originally were informative aspects for the signaler, but not necessarily mate attraction signals might only
of the signaler and then were further for the recipient)? If signaler and be produced by males that are of
specialized over evolutionary time to recipient have aligned interests, then sufficiently high quality, because
convey information more effectively. this problem of manipulation does not the costs to lower quality males of
There is also another route for arise; but if signaler and recipient have displaying these signals would be
the evolution of signals: ‘recipient conflicting interests, then manipulation prohibitive. Parallel concepts had
precursors’. In this case, recipients can be a problem. In a seminal paper, arisen independently in economics,
may have preexisting sensory biases Richard Dawkins and John Krebs where ‘conspicuous consumption’
that are either accidental or have suggested that, from an evolutionary and ‘extravagant wastefulness’ were
been selectively favored in contexts perspective, signals should be viewed suggested to reliably signal wealth
independent of communication. For as manipulative, as natural selection among humans. For the handicap
instance, females of a certain species will always favor signalers that elicit principle, in particular, the long train
might prefer and be attracted to the responses that are in their own selfish of the peacock seemed to provide a
color red because their preferred interests, regardless of the fate of the plausible example, given the expense
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situations, therefore, typically hinge

Box 3. on the fact that recipients of signals
have their own evolutionary interests,
Factors guaranteeing signals remain reliable despite signaler–recipient conflict.
so if signals do become unreliable,
then it will no longer pay recipients
Index: these signals (sometimes referred to as ‘unfakeable’ or ‘assessment’ signals) are
to attend to them. The tendency of
intrinsically anchored to an animal’s anatomy or physiology by physical constraints. Such
recipients to ignore unreliable signals
signals are usually based on some structure that has been grown over an extended period
should consequently put pressure
and which allows recipients to assess the signaler’s resource-holding potential. The cost
on signalers to use only the types of
that stabilizes reliability is thus paid over the course of development, such as through
signals that can be readily validated,
investment in size or generation of a specific bodily organ. An example of index signals is
the frequency of vocalizations in frogs, where pitch depth is constrained by the mass of the
based on differential signaling costs
vocal chords, providing a reliable indicator of size.
or benefits or based on the past
signaling record of the signaler.
Quality handicap: these signals are the type first envisioned by Zahavi in which the cost Signalers and recipients will thus be
that stabilizes honesty is paid as the signal is produced. These signals ‘use up’ the quality dynamically coupled over time — even
being advertised — often because they are energetically costly — so only ‘high quality’ if one party attains an advantage for
individuals can afford them. An example of quality handicap signals is the roaring of red some period, over the long haul we
deer, where the production of roars requires significant and prolonged movement of chest should expect signalers to provide
muscles and thus quickly exhausts ‘low quality’ individuals. reliable information, and recipients
to make use of this information, with
General handicap: these signals incur a production cost, but this cost is the same for all both parties benefiting overall from
signalers. What differs between signalers is the benefits they stand to gain from success- their co-evolutionary relationship.
fully eliciting a response with the signal. Signalers that will benefit more (e.g., hungrier off- An important subtlety though is
spring) are more likely to signal (e.g., beg more often for food from their parents), indicating that while signals are predicted to be
their greater need. An example of general handicap signals are the gaping mouth displays generally reliable they need not be
produced by begging chicks of many bird species. perfectly reliable for recipients to still
pay attention to them. As long as
Convention and vulnerability: these signals can be produced with minimal production signals are ‘honest on average’ —
costs and negligible difficulty. Their reliability is guaranteed by the fact that recipients that is, they contain enough useful
frequently test signalers, probing them for weaknesses. Performance of some of these information for recipients to be better
signals thus places the signaler at risk, either by exposing a vulnerable part of the body off attending to them than ignoring
or precipitating attack. Individuals that perform these signals probabilistically suffer the them — then the signaling system
potential for severe injury, so those who would be unable to bear the associated risk would can remain evolutionarily stable.
find dishonesty unprofitable. An example are the black facial patterns (so-called ‘badges of Consequently, there is still scope for
status’) of paper wasps. signalers to occasionally misrepresent
their signals, with at least some
Reputation: these signals are not necessarily difficult or costly to produce, nor are they dishonesty occurring at equilibrium.
associated with attacks from recipients. These signals require only that signalers and recipi- As Wolfgang Wickler noted, “We
ents have prior knowledge of one another’s past signaling record, which occurs if individuals can really learn the truth about the
recognize one another, interact repeatedly, and remember the outcome of prior interactions.
evolution of signals best from the
Signals produced by individuals who were dishonest in the past will be devalued or not
liars.” Thus, as long as deception either
responded to at all. Potential cheaters thus experience a tradeoff between the immediate
remains at a low enough frequency,
benefits of successful dishonesty and the future consequences of losing their long-term
is difficult for recipients to detect, or
credibility. An example of a reputation signal is alarm calling in vervet monkeys, where indi-
does not harm recipients’ fitness too
viduals whose alarms have been unreliable in the past fail to evoke responses later on.
drastically, it can persist. Interestingly,
in stomatopod crustaceans, high levels
of threat displays are observed when
of growing and displaying such a be informative over evolutionary time signalers are molting — a life stage in
costly structure for its bearer. Yet, (Box 3). Indeed, when signalers and which the signaler is unable to follow
the question remained whether the recipients are highly related to one through with its threat, so that the
handicap principle could solve other another, or when they have minimal threat amounts to a bluff. Recipients
cases of conflicts-of-interest between conflicting interest, then signals nevertheless still flee from such bluffs.
signalers and recipients; and if not, may be cost free, with certain types The reason bluffing remains stable is
whether there might be other solutions of ‘pooling equilibria’ emerging in because only a small proportion of
for signal reliability. which some signalers of different individuals are molting at any one time;
types employ the same cost-free threat displays overall are therefore still
Solutions for signal reliability signal. And even when signalers and worth heeding, particularly because
Recent work has indicated that the recipients have strong conflicts of the costs to recipients of challenging
handicap principle is not the only interest, theoretical models indicate true threats can be extremely high.
possible explanation for the reliability that honesty itself need not be costly: Interestingly, in other systems, such as
of animal signals and, in fact, several all that is required is that each instance paper wasps, where black facial spots
mechanisms — not all of which require of lying that deviates from the honest of varying size and shape are ‘badges
excessive production costs — may equilibrium be met with high costs. of status’ that signal dominance,
guarantee that signals continue to Mechanisms for reliability in conflict wasps whose facial patterns do not
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reliably reflect their true dominance are female attention, so combinations of It is notable that many aspects
severely punished; and because high signals might synergize and exceed of human communication still have
status individuals are frequently tested the effectiveness of any single signal parallels with animal signals, being
in this system, bluffing is rare. component. based on non-verbal gestures or facial
expressions that are also found in our
Sexually-selected signals with Interactive experimental approaches primate relatives. Some researchers
multiple components While observation remains an essential have even suggested that gestures
Given the mechanisms favoring first step in describing animal signals, might have provided the first proto-
signalers that provide reliable experiments are critical for testing the languages during human evolution;
information, an important goal of accuracy of these conclusions and and it is interesting in this respect
studying animal signals is to isolate fully understanding the complexity that attempts to teach aspects of
the specific information content of of animal signals. A wide range language to nonhuman primates first
signals. This goal is perhaps most of experimental approaches have met with success only after American
challenging in mate choice, where been used to study animal signals, Sign Language — a gesture based
elaborate signaling traits have been though perhaps most useful are those system — was used. Nevertheless,
shaped by sexual selection and involving the interactive presentation of human language is far richer in its
can involve multiple components signals to live animals — what Donald communicative potential than any
and modalities (e.g., males courting Griffin has called “an experimental nonhuman species can attain, even
females by producing bright visual dialogue”. Such dialogues can be after dedicated training with human
colors, sounds, substrate-borne accomplished for signals from any teachers, and this therefore raises an
vibrations, and pheromones, all modality by presenting the signal to important challenge for research at the
simultaneously). An important recipients in controlled conditions (for interface of animal signals and human
question for such signals is how instance, through acoustic playback of language: how and why did language
recipients integrate all this complexity sound signals). Interactive models and arise as a communication system and
and how they use this information robots, in particular, offer a powerful why is it that no other animal signaling
to select mates. Two important means of isolating the responses that system has the power of human
hypotheses have been proposed signals elicit in recipients as well as language?
for such multi-modal sexual signals: the conditions under which signals
different signals might each convey are most likely to be produced. For Further reading
different information (the ‘multiple instance, the development of an Bergstrom, C.T. and Lachmann, M. (1998). Signaling
among relatives. III. Talk is cheap. Proc. Natl.
message’ hypothesis) or different interactive female sage grouse robot, Acad. Sci. USA 95, 5100–5105.
signals might convey the same with a camera and microphones Bradbury, J.W. and Vehrencamp, S.L. (2011).
Principles of Animal Communication, 2nd edition,
information (the ‘backup message’ implanted inside the robot, has (Sunderland, MA: Sinauer Associates).
hypothesis). It is also possible that enabled researchers to examine Hurd, P.L. (1995). Communication in discrete action-
some sexually selected signals how male sage grouse change their response games. J. Theoret. Biol. 174, 217–222.
Johnstone, R.A. (1997). The evolution of animal
might not provide information at all, courtship signals based on a female’s signals. In Behavioural Ecology: an Evolutionary
because they are still in a ‘runaway’ orientation and postures. Such Approach, 4th Edition, J.R. Krebs and N.B.
Davies, eds. (Oxford: Blackwell Science), pp.
process of exploitation that has research can give insights into how 155–178.
not yet stabilized. Researchers signalers coordinate their signaling Laidre, M.E. (2009). How often do animals lie about
are beginning to understand how with moment-by-moment feedback their intentions? An experimental test. Am. Nat.
173, 337–346.
these different explanations might from recipients. Macías Garcia, C. and Ramirez, E. (2005). Evidence
apply across animal species by that sensory traps can evolve into honest signals.
Nature 434, 501–505.
experimentally altering certain signal From animal signals to human Maynard Smith, J. and Harper, D. (2003). Animal
components and determining what language Signals (Oxford: Oxford University Press).
information recipients glean from them While animal signals can be Searcy, W.A. and Nowicki, S. (2005). The Evolution
of Animal Communication: Reliability and
and how they alter their response. complicated, they are dwarfed in Deception in Signaling Systems (Princeton, NJ:
Another useful approach has been to complexity by human language. Princeton University Press).
Seyfarth, R.M., Cheney, D.L., Bergman, T., Fischer, J.,
carefully measure the specific signal Language allows our species to Zuberbühler, K., and Hammerschmidt, K. (2010).
components that recipients attend transmit vastly more information than The central importance of information in studies
to most. For instance, researchers any animal signaling system and to of animal communication. Anim. Behav. 80, 3–8.
Slater, P.J.B. (1983). The study of communication.
recently developed a portable eye- communicate on any topic, new or In Animal Behavior, Communication, Vol. 2,
tracking system to examine which imaginary. Humans can accomplish T.R. Halliday and P.J.B. Slater, eds. (New York:
W.H. Freeman), pp. 9–42.
elements of a peacock’s multi- this feat because we are able to Tibbetts, E.A. (2008). Resource value and the context
ornament display are visually attended semantically reference anything dependence of receiver behaviour. Proc. Roy.
to by females. Interestingly, females around us with words and then create Soc. B 275, 2201–2206.
Yorzinski, J.L., Patricelli, G.L., Babcock, J.S.,
selectively attended to specific new meanings based on the unique Pearson, J.M., and Platt, M.L. (2013). Through
components of male’s courtship syntax of altered word-orderings. In their eyes: selective attention in peahens during
courtship. J. Exp. Biol. 216, 3035–3046.
displays and largely ignored other contrast, animal signals are often,
components, which suggests some though certainly not always, single
1Department of Integrative Biology,
components might be differentially isolated signals or repeated sets of the
University of California, Berkeley, USA.
informative. Notably though, the same signal, and they are generally 2Department of Zoology, University of
interaction between different signal dedicated to specialized functions Cambridge, UK.
components sometimes functioned to that provide just a few categories of E-mail: mlaidre@berkeley.edu,
more effectively capture and maintain information. raj1003@hermes.cam.ac.uk