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Alarm Calling

Alarm Calling
Mélissa Berthet
and Klaus Zuberbühler
Institut Jean Nicod, Département détudes
cognitives, ENS, EHESS, CNRS, PSL Research
University, Paris, France
Institute of Biology, University of Neuchatel,
Neuchatel, Switzerland
School of Psychology and Neuroscience,
University of St Andrews, St Andrews, UK
Alert calling;Antipredator calling;Distress call-
ing;Mobbing calling
Vocal behavior emitted in response to a threaten-
ing situation
The term alarm calling is used to refer to an
acoustically diverse group of animal vocaliza-
tions, emitted in response to some threatening
event, usually a predator. Alarm calling is wide-
spread among social animals, although most data
are from primates, rodents, and birds.
Evolutionary Function
This behaviour is puzzling from an evolutionary
perspective. The term is used to refer to an acous-
tically diverse group of animal vocalizations,
emitted in response to some threatening event,
usually a predator. Alarm calling is widespread
among social animals, although most data are
from primates, rodents, and birds. Why should
an individual vocalize in the presence of a preda-
tor and hereby reveal its location and attract atten-
tion? How can such seemingly maladaptive
behavior evolve?
Different non-exclusive hypotheses have been
proposed to explain the evolution of this seem-
ingly paradoxical behavior (Stephan and
Zuberbühler 2016). They differ both in terms of
the presumed beneciary (selsh vs. altruistic
alarm calling) and in terms of the targeted recipi-
ent (predator vs. conspecics).
Selfish Alarm Calling
One group of hypotheses presumes that alarm
calling is directly benecial to the caller, either
because it impacts on the predator or because it
induces behavior in other prey that is benecial to
the caller. First, alarm calls can signal detection to
a predator, the perception advertisement
hypothesis. This strategy is particularly effective
with predators that hunt by surprise and abandon
hunting after detection. The hypothesis can also
explain alarm calling by lone individuals and non-
social species. Related to this is the pursuit-
© Springer Nature Switzerland AG 2020
T. K. Shackelford, V. A. Weekes-Shackelford (eds.), Encyclopedia of Evolutionary Psychological Science,
deterrence hypothesis, put forward to explain
stotting behavior in ungulates, a visual alarm sig-
nal that showcases a preys superior locomotor
capacities and the futility of pursuit.
However, selsh alarm calling is not always
aimed at the predator. Under the prey manipula-
tion hypothesis, alarm calling functions to trigger
escape behavior in other prey, which creates gen-
eral pandemonium that distracts the predator and,
as a consequence, increases the callers own sur-
vival changes. Under the cooperative defense
hypothesis, alarm calling is also aimed at other
prey, but to trigger predator approaching and chas-
ing (mobbing), which increases the likelihood
of the callers own survival.
Altruistic Alarm Calling
A second group of hypotheses presumes that
alarm calling evolved to benet the caller indi-
rectly by favoring genetic relatives and other valu-
able group members. Under the kin selection
hypothesis, alarm calling provides genetic advan-
tages to a caller, which is the case if the caller is
surrounded by own offspring or other closely
related individuals. Following Hamiltons rule,
alarm calling can evolve even if it is costly to the
signaller, provided it sufciently benets genetic
relatives. In some species, there is evidence that
callers maximize their indirect tness benets by
taking the audience into account, for instance, by
alarm calling more in the presence of young and
vulnerable offspring than other audiences (e.g.,
yellow-bellied marmots, Blumstein 2007).
Finally, costly alarm calling may also evolve if
it favors a callers reproductive success by pre-
serving mating opportunities, the sexual selection
hypothesis. This argument has been made for
adult males in polygynous species. For example,
in Diana monkeys males produce acoustically
highly conspicuous alarm call that carry over
long distances, much beyond what is predicted
for communication to the predator or other group
members, suggesting that male alarm calls operate
in male-male competition and female choice.
However, this is most likely a secondary evolu-
tionary process, by which already existing alarm
calls are subject to the forces of sexual selection to
take on an additional function in reproduction.
Information Content
Call Production
What kind of information is encoded in animal
alarm calls? Communication involves at least two
partners, a signaller and a recipient, which may
experience different processes. First, the acoustic
structure of alarm calls is determined by the
shape of the signallers vocal tract, which pro-
vides recipients with reliable information about
the callers body size, age, sex, and identity
(Bowling et al. 2017). In addition, psychologi-
cally relevant events often have physiological
effects, such as changes in heart rate, skin temper-
ature, or hormone levels, which create further
variation in a signallers vocal tract shape and,
consequently, the acoustic quality of alarm calls,
Mortons motivational-structural rules (Morton
1977). Since this process is determined by a cal-
lers prior experience with an event, call produc-
tion is also under cognitive control.
Call Comprehension
Recipients, on the other hand, may either be
directly affected by the acoustic structure of
alarm calls (Owren and Rendall 2001), or they
have learned about the referential relations
between alarm call types and events (Schlenker
et al. 2016). One ongoing debate is about the
nature of the mental representations, or memories,
that mediate between alarm calls and events
(Seyfarth et al. 2010). If an alarm call is only
given to a narrow set of situations, listeners can
directly infer the eliciting event, even in the
absence of further cues, to the effect that the call
obtains something akin to lexical meaning. How-
ever, most studies are unable to pin down more
specically what type of information is conveyed,
such as the type, behavior, or distance of the
predator, and many alarm calls are given to a
range of situations that do not share clear
similarities at least from a human perspective
(Dezecache and Berthet 2018). Here, listeners
appear to rely on pragmatics to identify the
event that has caused the call. A number of play-
back studies have tested this idea and produced
evidence that referentially broad alarm calls can
obtain relatively specic meaning during a
2 Alarm Calling
process by which listeners can associate the call to
a range of possible events and then choose among
the most probable one. Also, some species use
social knowledge to react to othersalarm calls.
For example, vervet monkeys react less strongly
to alarm calls given by juveniles, possibly because
they give alarm calls to wider range of distur-
bances than adult monkeys that only call in cases
of real danger.
Call Sequences: Temporal and Morphological
Alarm calls are often emitted in sequences, raising
the possibility that information could be conveyed
by resulting structural differences, such as due to
variation in temporal structure. This is the case for
titi monkeys that emit alarm calls more regularly
in predator-related than non-predator-related
sequences. In black-capped chickadees, call rate
differences also exist, but here they have been
linked to size differences of predators. Another
relevant example is alarm call sequences in black-
and-white colobus and guereza monkeys, which
produce sequences of few roars when encounter-
ing leopards and many roars when encountering
crowned eagles, a difference discriminated by
Second, alarm call sequences sometimes con-
sist of different call types, which result in
sequences that qualify as ordered permutations
or unordered combinations (Zuberbühler in
press). An example of call combinations is titi
monkeys combining A and B alarm calls into
sequences, whereby the proportion of B-call com-
binations reliably encodes predator type and
An example of a permutation is male
Campbells monkeys combining krakalarms
(typically given to leopards) and hokalarms
(typically given to eagles) with an acoustically
invariable vocal unit (oo) in cases of non-
imminent danger. Recipients discriminate krak
from krak-oo alarms, suggesting that oo per-
forms a semantic operation. The system thus
resembles a common operation in human lan-
guage, afxation, whereby an utterance with lex-
ical meaning is combined with a meaningless
afx, to generate a derived meaning.
Another example of a permutation is male
Campbells monkey boomcalls, produced
prior to subsequent krak-oos, whenever the dis-
turbance is non-predatory (e.g., falling tree). In
playback experiments, Diana monkeys discrimi-
nated alarm sequences with and without preced-
ing booms, suggesting that the booms altered the
meaning of the sequence.
Permutations have also been found in putty-
nosed monkeys. Here, males produce series of
pyows to terrestrial disturbances and series of
hacks to crowned eagles. In addition, males some-
times add brief combinations of several pyows,
followed by several hacks. The pyow-hack tran-
sition appears to carry its own meaning, unrelated
to the meaning of the constituent parts, by
announcing forthcoming group movement. The
pyow-hack transition hence resembles an idio-
matic expression, i.e., the meaning of the call
combination cannot be derived from the meaning
of its parts, similar to English expressions such as
raining cats and dogs,i.e., raining heavily.
An important discussion is whether any animal
call sequence qualies as truly compositional
(Townsend et al. 2018). Compositionality is a
dening feature of human language whereby the
meaning of an expression is determined by the
meaning of its parts and the rule that combines
them. Some of the best current examples of animal
compositionality come from studies on bird alarm
calls. For instance, Japanese tits possess alert
calls that warn conspecics about the presence of
predators and recruitmentcalls that attract con-
specics in non-dangerous situations, for exam-
ple, to food. When mobbing a predator, however,
tits combine the two calls to alert-recruitment
sequences, which engage nearby conspecics into
cooperative antipredator behavior. Interestingly,
reversed sequences do not elicit mobbing behav-
ior, suggesting that the system is both permuta-
tional and compositional (Zuberbühler in press).
Alarm Calling 3
Ontogeny and Learning
How do animals acquire their alarm calls? Most
ontogenetic studies of alarm calls have focused on
recipients, i.e., how animal learn to comprehend
the meaning of alarm calls. In many species,
infants appear to be born with partly innate knowl-
edge of alarm calls. For example, newborn ground
squirrels react to conspecic alarm calls by freez-
ing or increasing vigilance. Similarly, cross-
fostered dunnocks cease to beg for food when
hearing conspecic, but not foster parent alarm
calls. Nevertheless, their response is weaker com-
pared to normally raised chicks, suggesting that
learning plays a moderating role (Hollen and
Radford 2009). In many species, however, alarm
call comprehension is subject to social learning.
Social learning is highly adaptive, especially in
acquiring antipredator behavior, as it protects
infants from committing fatal errors. For example,
infant meerkats that have stayed close to adults are
more likely to respond appropriately to alarm calls
than other infants.
Research on the ontogeny of alarm call production
is more limited. Generally, learning appears to
have only minor effects on the acoustic structure
of alarm calls. For example, in species such as
yellow-bellied marmots, great gerbils, and meer-
kats, juvenile and adult alarm calls are nearly
identical. Partly, this may be because the acoustic
structure of animal alarm calls itself has been
under strong selection pressure. For example,
bird raptor alarms are often difcult to localize
(presumably to prevent detection), whereas mon-
key leopard alarms are highly conspicuous
(presumably to promote dissuasion). A notable
exception is the fork-tailed drongo that, in addi-
tion to its own species-specic alarm calls, is able
to mimic other speciesalarm calls, although this
ability functions in deceptive foraging.
Call use, nally, appears to be more plastic, but
again relatively little work has been carried out. As
a basic principle, infants must learn to recognize the
dangerous species, which can happen through a
process of either elimination or addition. For exam-
ple, young vervet monkeys begin by giving alarm
calls to a broad range of stimuli, including non-
predatory species (e.g., ying pigeons), albeit in a
nonrandom manner: eagle alarms are produced to
ying animals, leopard alarms to terrestrial species,
and snake alarms to snake-like objects. This has also
been demonstrated in monkeys experimentally
exposed to unfamiliar threat. For example, green
monkeys exposed to a drone will produce alarm
calls that resemble vervet monkey eagle alarms.
The inverse process has been described in infant
chimpanzees that do not appear to have any pre-
existing knowledge of alarm call use but learn by
observing others interacting with unfamiliar threats.
Alarm calling is of importance to various scien-
tic disciplines, including evolutionary theory,
behavioral ecology, animal cognition, compara-
tive linguistics, and philosophy of mind. They
are relatively uncomplicated to work with and
easily recognizable, due to their context specic-
ity and unique acoustic structure. They have been
essential in addressing a range of basic questions,
such as the evolution of altruism, the behavioral
ecology of predator-prey relations, and the evolu-
tion of animal cognition. Detailed behavioral ana-
lyses, based on naturalistic observations and
experiments across a wide range of species, have
produced much progress and provided a window
into the animal mind and some of the basic forces
that drive evolution.
Alarm Call Creates Confusion
Alarm Caller may be Parent
Alarm Caller Targeted by Predator
Alarm Callers Genes Represented in
Alarm Calling and Kinship
Alarm Calling Predicted by Inclusive Fitness
Alarm Calling Upon Predator Detection
4 Alarm Calling
Alarm Calls
Predator Confusion Hypothesis
Predator Mobbing
Blumstein, D. T. (2007). The evolution of alarm commu-
nication in rodents: Structure, function, and the puzzle
of apparently altruistic calling. In J. O. Wolff & P. W.
Sherman (Éd.), Rodent societies: An ecological & evo-
lutionary perspective (University of Chicago Press,
p. 317327). Chicago and London.
Bowling, D. L., Garcia, M., Dunn, J. C., Ruprecht, R.,
Stewart, A., Frommolt, K. H., & Fitch, W. T. (2017).
Body size and vocalization in primates and carnivores.
Dezecache, G., & Berthet, M. (2018). Working hypotheses
on the meaning of general alarm calls. Ani Behav, 142,
Hollen, L. I., & Radford, A. N. (2009). The development of
alarm call behaviour in mammals and birds. Animal
Behaviour, 78(4), 791800.
Morton, E. S. (1977). On the occurrence and signicance
of motivation structural rules in some bird and mam-
mal sounds. American Naturalist, 111, 855869.
Owren, M. J., & Rendall, D. (2001). Sound on the rebound:
Bringing form and function back to the forefront in
understanding nonhuman primate vocal signaling. Evo-
lutionary Anthropology, 10,5871.
Schlenker, P., Chemla, E., & Zuberbuhler, K. (2016). What
do monkey calls mean? Trends in Cognitive Sciences,
20(12), 894904.
Seyfarth, R. M., Cheney, D. L., Bergman, T., Fischer, J.,
Zuberbuehler, K., & Hammerschmidt, K. (2010). The
central importance of information in studies of animal
communication. Animal Behaviour, 80(1), 38. https://
Stephan, C., & Zuberbühler, K. (2016). Alarm calling and
kinship. In V. Weekes-Shackelford, T. K. Shackelford,
& V. A. Weekes-Shackelford (Eds.), Encyclopedia of
Evolutionary Psychological Science. Switzerland:
Townsend, S. W., Engesser, S., Stoll, S., Zuberbuhler, K.,
& Bickel, B. (2018). Compositionality in animals and
humans. PLoS Biology, 16(8).
Zuberbühler, K. (in press). Syntax and compositionality in
animal communication. Philosophical Transactions of
the Royal Society of London B.
Alarm Calling 5
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The evolution of alarm communication in rodents : Structure, function, and the puzzle of apparently altruistic calling
  • D T Blumstein
Blumstein, D. T. (2007). The evolution of alarm communication in rodents : Structure, function, and the puzzle of apparently altruistic calling. In J. O. Wolff & P. W. Sherman (Éd.), Rodent societies : An ecological & evolutionary perspective (University of Chicago Press, p. 317-327). Chicago and London.