Alarm Calling and Kinship
KeywordsSexual Selection Alarm Call Inclusive Fitness Vervet Monkey Antipredator Behavior
Vocal behavior of prey animals to defend themselves and others from predation.
Alarm calling is a widespread phenomenon in the animal kingdom, usually produced by individuals during predation attempts, a context with large fitness consequences, suggesting that the behavior has been under strong selection pressure. But there is something paradoxical about animal alarm calls. Why should an individual, faced with a potentially lethal predator, behave in conspicuous ways to warn others, rather than trying to escape or hide from the danger? This seemingly altruistic behavior has posed a major challenge for evolutionary theory and become the topic of countless studies. Two major research themes have been addressed with studies on animal alarm calls: the cognitive processes involved in call production and perception and the evolutionary forces that have shaped the behavior. The following sections review some of the current research trends in both areas.
The Cognition of Animal Alarm Calls
In many species, alarm calls seem to “stand for” something in the external world, which has raised questions about potential parallels to human language and the idea that alarm calls are useful to investigate cognitive processes underlying vocal communication. However, this line of research has remained controversial, mainly because of difficulties in describing the nature of the internal processes triggered by external events. Discussions often revolve around how “cognitive” these internal processes and psychological states are, for example, whether predatory events merely trigger specific emotions (e.g., fear) to which alarm calls are hardwired. Empirical support for this position comes from studies showing that animals sometimes give alarm calls to non-predatory situations, such as putty-nosed monkeys (Cercopithecus nictitans) and other primates producing “eagle” alarms to falling trees or baboon fights, as well as “terrestrial predator” alarms to a wide range of disturbing events, which include encounters with non-predators.
Also relevant is that, in many species, alarm calls show only limited acoustic flexibility. In birds, alarm call structure is often highly conserved across species, especially to aerial predators (Marler 1955). One hypothesis is that these aerial alarms have evolved to conceal the location of the signaler by limiting sound propagation and directional cues (for review, also see Marler 2004). For example, the “seet” alarms of many bird species appear to be a hardwired response to the limited auditory range of raptors, which limits the amount of information a signaler can encode in this call type.
Some other studies, however, have found more flexibility in alarm calling behavior with sometimes tight relationships between external events and corresponding signals, including event-specific differences in acoustic structure, call rates, or sequential organization of calls. For example, in several species it has been shown that not only predator type but also predator size, predator distance, and predator behavior can trigger distinct alarm call behavior, suggesting that some animals can represent external events in complex ways and have means to communicate them to their nearby audiences. Here, a particularly interesting line of research has been to look at sequences of alarm calls. Although many primate and non-primate species have restricted vocal repertoires with rigid call structures, some species appear to have overcome this limitation by producing call sequences of different composition that are sometimes linked to specific external events. Differences in perceived urgency can also lead to different call combinations, with information about external events sometimes additionally included.
A second controversy concerning the internal states associated with animal alarm calling revolves around the question of whether animals give alarm calls with the intention to inform others. Human language appears to be built on this principle, insofar as speakers convey mental content that is directed at particular partners and largely for their benefit, after relevant judgments that can be rather complex (Sperber 1986). The alternative extreme position to this view is that callers do not understand what they communicate, but that selection has equipped them to produce specific signals in specific situations, with callers remaining oblivious to the social consequences of their behavior.
One way to address this second controversy is to study the impact of the audience on an individual’s alarm calling behavior. Although not fully clarified, results so far suggest that, in chimpanzees (Pan troglodytes), alarm vocalizations are not mere automatically triggered utterances but indeed represent a means to communicate the nature of a danger to others. However, there is also important negative evidence, such as female vervet monkeys (Cercopithecus aethiops) failing to use alarm calls to change the knowledge state of their offspring in dangerous situations. For the time being, the underpinning cognitive processes of animal alarm calling, especially its intentional nature, remain nebulous for many species, with no clear phylogenetic trends.
A third research theme centers on considerations about the other end of a communicative interaction, the cognition involved in processing alarm calls. One basic question here is whether receivers react directly to the physical features of calls (e.g., Rendall et al. 2009) or whether this is mediated by a mental representation of the call-eliciting event, i.e., whether calls carry specific information for the recipient (Seyfarth et al. 2010). Although more research needs to be done, there is some evidence that predator alarm calls in primates elicit responses due to their referential links to external events, not because of their physical features. In primates, predator alarm calls can trigger specific anticipations in recipients, suggesting that they do more than just spreading a motivation within a group, but possibly activate a relatively specific mental representation of the predator normally associated with the alarm call.
If receivers are able to extract and encode information when hearing a call, then another question is whether they infer the same information that the signaler originally responded to and whether they take the identity of the caller into account. Here, more progress has been made, largely due to the relative ease with which receivers can be tested with field experiments. An emerging pattern is that animals typically take the identity of the caller into account, as well as the pragmatic circumstances of a call-eliciting event.
In sum, current evidence is in line with the more general hypothesis that signalers and receivers are driven by different internal states and that there is a cognitive disparity between them. Thus, unlike in human language, producing and comprehending alarm calls might be linked to different cognitive underpinnings that probably followed different evolutionary pathways but are, nonetheless, often taking place in the same individual. However, more research is needed here to address this problem more directly.
The Evolution of Animal Alarm Calling
The second major research topic with animal alarm calls concerns the question of why it is adaptive for an individual to produce conspicuous vocalizations that reveal its presence and location to a dangerous predator and, as a result, increase predation risk. The prediction here is that alarm calling must have some beneficial effects for the caller that outweigh the obvious costs incurred; otherwise, selection would have acted against it.
Three levels of selection have been identified to explain the evolution of alarm calling, i.e., alarm calling to enhance the caller’s own survival (individual selection), the survival of its relatives (kin selection), or its reproductive success (sexual selection). If a caller can accrue benefits due to one or several of these forces, then the costs of alarm calling might be outweighed, and selection will favor the behavior, according to “Hamilton’s rule” (Hamilton 1963). It is important to consider that the three levels of selection are by no means mutually exclusive but represent three possible ways by which an individual can maximize its genetic contribution to future generations, as follows.
Individual Selection: Alarm Calling to Enhance Signaler Survival
Although alarm calls generally reveal a caller’s location, they can have a number of secondary beneficial effects, namely, by impacting on the behavior of other animals, in ways that increase the probability to survive for the signaler. Two main mechanisms have been identified, a direct one by influencing the predator’s hunting behavior (“perception advertisement” or “pursuit deterrent” hypotheses; Frankenberg 1981) and an indirect one by influencing other prey’s antipredator behavior (“prey manipulation” hypotheses; Charnov and Krebs 1975).
Some predators rely on stealth and experience, and experience significantly reduced hunting success if prey animals are aware of their presence. Signaling perception to a predator can therefore be adaptive if the predator is likely to abandon a hunting attempt and move on to target other individuals. If alarm calls have a predator-deterring function, then the prediction is that a predator’s hunting behavior must change in response to alarm calls. In one study, forest leopards, “Panthera pardus” were radio-tracked, and the resulting ranging data revealed that forest leopards hunted by approaching monkey groups to hide in nearby vegetation, apparently to wait for unaware individuals to descend. Data also showed that leopards abandoned their hiding positions soon after detection by alarm calling monkeys, often additionally accompanied by approaching the predator directly.
However, most animals are hunted by a range of predator species that differ considerably in their hunting strategies, to the effect that alarm calls only work as a perception advertisement signals for some but not other predators.
The perception advertisement hypothesis therefore presupposes some relevant cognitive capacities on behalf of the prey, insofar as callers not only have to discriminate predator classes but also need knowledge about their respective hunting strategies, in order to adjust their alarm calling behavior accordingly. African forest monkeys, for example, readily produce loud alarm calls to two of their predators, leopards and crowned eagles, but remain silent to two other major predators, chimpanzees and humans, and there is evidence that the different antipredator strategies are learned. In a study on Diana monkeys, “Cercopithecus diana” in Taï National Park, Ivory Coast, it was shown that groups in the center of a chimpanzee territory behaved differently to the simulated presence of chimpanzees compared to groups living at the periphery of a territory (Zuberbühler 2000). Chimpanzees spend the majority of time in the core area of their territories and only occasionally venture into the peripheral parts. As a result, monkey groups in the center of a chimpanzee territory will have more experience with chimpanzee behavior than monkey groups living in the periphery. Chimpanzees also face predation pressure by leopards and, when encountering a leopard, respond with specific calls (“SOS” screams). In one experiment, chimpanzee SOS screams to leopards were broadcasted to different groups of Diana monkeys. As predicted, groups in the center of chimp territories responded more often with their own leopard alarms than groups in the periphery, who mostly responded cryptically with no signs that they could discriminate the chimpanzee SOS screams from screams given during fights with other group members. The most likely interpretation is that peripheral Diana monkeys had fewer opportunities to observe chimpanzees responding to leopards compared to central groups and were thus mostly prevented from learning the meaning of the different chimpanzee calls.
Many animals are hunted by aerial predators and have evolved acoustically distinct alarm calls to defend themselves. For example, crowned eagles (Stephanoaetus coronatus) are specialized primate predators. Although they can sometimes be deterred by alarm calling monkeys, often in combination with physical attacks by adult males (KZ and CS, unpublished data), they remain extremely dangerous for monkeys, with attacks sometimes happening several times per day. Crowned eagles typically hunt by sitting and waiting in the upper forest canopy for an approaching group of monkeys. Their attacks are sudden and at short range by launching upon an individual from their perch. If unsuccessful they can engage in prolonged hunting efforts on a group of monkeys, sometimes by hunting in pairs, suggesting that callers must gain benefits other than perception advertisement when alarm calling to aerial predators.
In sum, although alarm calls can have dissuasive effects on some predators or in some situations, perception advertisement and predator deterrence cannot fully account for the evolution of animal alarm calls.
A caller’s probability to survive a predation attempt can also increase if alarm calls trigger behavior in other prey animals that benefits the caller or that leads to more efficient antipredator responses. For example, if alarm calls trigger flight in others, a predator may find it more difficult to focus on the caller, who can benefit from “safety in numbers” (Bednekoff and Lima 1998) or “confusion” effects (Milinski and Heller 1978). While safety in numbers simply decreases the probability of being caught due to stochastic processes (a dilution effect), the confusion effect relates to increased capture time for a predator (and thus an increased probability to escape for prey), possibly due to a sensory overload of chaotic movements during flights. If alarm calls trigger such movements, the caller will benefit not only from dilution but also from confusion effects.
However, alarm calls may also induce collective antipredator behavior, such as predator mobbing. This can occur if calling attracts others for a communal antipredator response, in line with the etymological origin of alarm as “all’arme” (= to arms). Alarm call-induced cooperative defense can be observed in many species (Curio 1978), but it can also occur in hetero-specific associations, for instance, between males of different guenon species living in polyspecific groups. Predators are often repelled by mobbing groups of prey animals, most likely because they are prevented from carrying out their preferred hunting strategy.
A third direct benefit of alarm calling arises if callers can provide essential learning opportunities for less experienced individuals during predator encounters, which will increase the number of reliable sentinels for future predatory events, a mechanism that has been proposed for meerkats. In one classic experiment, Curio et al. (1978) conditioned naïve blackbirds to alarm call to a harmless object by social cues alone. The main manipulation consisted of presenting a demonstrator bird with a raptor model (to elicit alarm calls) in the presence of a second naïve bird. The observer bird did not see the call-eliciting raptor but was allowed to see a novel, but harmless, model during the conspecific’s alarm response. When retested, observers responded with alarm calling to the harmless object, suggesting that blackbirds learn antipredator behavior from conspecifics by observational learning, without a need for direct predator experience.
To conclude, individuals can gain direct fitness benefits from producing alarm calls to predators in two major ways, either by directly interfering with the predator or by causing a change in the audience, which lowers the predator’s hunting success, and effects may occur simultaneously during natural hunting events.
Alarm Calling to Favor Kin
Another main explanation for the evolution of alarm calls is to interpret them as a form of extended parental care, i.e., reproductive individuals alarm call to prevent predation on their offspring (Blumstein et al. 1997). A more general version of the same idea is that alarm calling is adaptive if this benefits other individuals with whom the caller shares a substantial proportion of its genome (Smith 1965). The kin selection hypothesis of alarm calls makes several testable predictions. Most importantly, the alarm calling behavior of an individual should be a function of the costliness of alarm calling, the benefits for listeners, and the (cumulative) relatedness between the caller and the nearby listeners, according to Hamilton’s rule. Moreover, solitary individuals should not vocalize (unless calls carry over long distances and benefit distant relatives).
Empirical support for these assumptions is surprisingly inconsistent. Female Siberian jays (Perisoreus infaustus) utter more alarm calls when with their own offspring compared to other conspecifics, but males give alarm calls regardless of their relatedness to other group members (Griesser and Ekman 2004). Alarm calls as form of parental care is sometimes also seen in males. For example, in blue monkeys (Cercopithecus mitis), the single males produced higher rates of alarm calls if their group members (including own offspring) were closer to a simulated danger than further away, regardless of the male’s own distance to the predator (Papworth et al. 2008). However, the effect was only observed for eagle not leopard-related dangers.
Evidence for an effect of non-descendant kin is generally rare. Exceptions are female Gunnison’s prairie dogs (Cynomys gunnisoni), calling more to terrestrial predators in the presence of non-descendent kin than other individuals, and similar effects have been reported for Belding’s ground squirrels (Spermophilus beldingi; Sherman 1985) in which anti-predation behavior toward terrestrial predators increased with the presence of non-descent kin, but no such effects were found to aerial predators. In contrast, Columbian ground squirrels (Spermophilus columbianus) showed increased anti-predation behavior in the presence of non-descent kin toward aerial predators and no effect of kinship toward terrestrial predators (Macwhirter 1992). Inconsistent patterns for the impact of kinship on alarm calling were also found in vervet monkeys. While captive females alarm called more in the presence of kin, it was also found that higher-ranking females called more than lower-ranking females, with no correlation between rank and the presence of kin (Cheney and Seyfarth 1985).
Finally, male Thomas langurs (Presbytis thomasi) and yellow mongooses (Cynictis penicillata) do not alarm call when alone (Wich and Sterck 2003; Le Roux et al. 2008), but solitary Campbell’s monkey, “Cercopithecus campbelli” males living in a polyspecific association with Diana monkeys have been observed to alarm call to predators (KZ, unpublished data).
However, kin selection may have favored other aspects of animal alarm calling, notably the evolution of individually distinct acoustic cues. In Belding’s ground squirrels, alarm calls not only encode identity, but the acoustic similarity between alarms is a function of genetic similarity (McCowan and Hooper 2002). Acoustic cues of kinship may provide receivers with important information to decide whether a caller should be helped during a predation attempt.
In conclusion, genetic relatedness appears to have influenced the evolution of alarm calling, but the link between the kinship and alarm calling is often unclear, most likely due to additional factors having impacted on the evolution of alarm calling (see previous section).
Alarm Call Evolution in Relation to Sex
A third way for an individual to increase its inclusive fitness during costly alarm calling is if the behavior enhances future access to mating partners and opportunities to sire offspring. Several studies suggest that alarm calling may function in this way, but along different pathways. First, alarm calling may function in intersexual selection, such as mates (usually males) advertising their quality to choosy partners. Second, alarm calling may function in intra-sexual selection as a way to compete for access to sexual partners. Interestingly, in forest guenons, it is mainly the single adult males that engage in conspicuous alarm calling, which can be heard far beyond the group boundaries, suggesting an additional function in male–male competition. If males differ in their ability to engage in predation defense, then females may choose group males accordingly, while their alarm calling behavior might serve as a cue for their genetic quality or physical condition. In primates, indirect evidence comes from gray-cheeked mangabeys (Lophocebus albigena) in which the highest-ranking males engage most actively in predator-mobbing behavior (Arlet and Isbell 2009), suggesting a link between antipredator behavior and reproductive success.
In various mammal taxa, vocal structures, such as call duration, fundamental frequency, or formant frequencies, are linked to body size and competitive strength, suggesting that female receivers should attend to these cues. For instance, female red deer hinds and female koalas attend to acoustic cues of vocalizations to infer and compare the males’ physical characteristics and momentary condition (Reby et al. 2010; Charlton et al. 2012). Other evidence comes from birds (e.g., Beecher and Brenowitz 2005) and anurans (e.g., Ryan and Rand 1990). Here, differences in the variability of notes, call rate, call intensity, or call duration in calling males appear to form the basis for female mate choice.
Whether or not sexual selection has been equally at work in alarm call evolution, however, is less clear. Many species produce alarm calls in sexually dimorphic ways, both at the level of call structure and call use. For instance, male vervet monkeys and male domestic chicken are more likely to alarm call in the presence of (unrelated) adult females than other individuals, which is predicted neither by kin nor individual selection. In red jungle fowls (Gallus gallus), male alarm call rates and mating frequencies are correlated, although this may be the result of differences in previous mating success rather than a way to increase a male’s attractiveness.
Some other relevant evidence in support of sexual selection comes from Diana monkeys, in which both sexes emit predator-specific alarms to leopards and eagles. Recent evidence has shown that males alarm call, not just to provide predator information to nearby group members and the presence to distant rivals but also to advertise to their own females their willingness to defend the group. When confronted with contradicting predatory information (e.g., perceiving a leopard followed by own females’ eagle alarm calls), males prioritize the information provided by the females and respond with eagle alarm calls, contrary to their own experience (Stephan and Zuberbühler 2016). In contrast, if females are presented with contradicting information, they ignore the male’s alarm calls and only respond to the predator they have witnessed themselves. Another effect was that, as soon as a male produced alarm calls that referentially matched the females’, the females stopped giving their own alarm calls. One interpretation of these findings is that, by referentially matching his alarm calls to the females’, the male signaled his readiness to engage with the predator identified by the females. In this view, the females used the male’s compliant behavior as kind of a “stopping rule” for own risky antipredator behavior. In sum, the study demonstrates an advanced coordination between the two sexes during predatory events, which goes beyond advertising mere physical condition and includes others’ assessments of external events and signaling readiness to engage with them. One likely evolutionary scenario is that males have been under sexual selection pressure to act this way. What remains to be tested is whether this type of coordinated alarm call behavior in males indeed leads to more surviving offspring. One prediction is that compliant males are more preferred as group males, have longer tenure, and sire more offspring than males that produce alarm calls in response to their own assessment.
Overall, differences in alarm calling between females and males are a widespread and well-known phenomenon, and vocal signals have been shown to provide direct means to access mating partner quality. The Diana monkey study mentioned before suggests another way by which sexual selection could have acted on male callers, beyond providing cues linked to physical condition, in that males use alarm calls to advertise their antipredator commitment. But how exactly females choose males based on variation in their antipredator commitments is subject to further investigation. One possibility is that their tenure as single group males is constantly at stake and that males who show decreased commitment over time will eventually be expelled and replaced by another male. Generally, polygynous systems are supposed to be especially susceptible to be targeted by sexual selection, and a sexual dimorphism in call structure and usage might give first hints on functional differences between male and female calls.
There is solid evidence that selection has acted in different ways on the evolution of alarm calls, contributing in various ways to the increase of an individual’s inclusive fitness. What is more difficult to show is how exactly costly alarm calling enhances a caller’s own survival, the survival of its kin, and its future reproducing success in different animal species. In all likelihood, selection has shaped alarm calling behavior in different ways and in a cumulative manner (Zuberbühler 2002). Predator deterrence benefits may have originally triggered the evolution of alarm calling behavior, but kin and sexual selection may have contributed additionally, in parallel with a species’ social evolution. Also important is that, even within species, selection may have acted differently on different age/sex classes causing differences in alarm calling behavior, as illustrated by, e.g., sex-specific patterns of alarm calling in Diana monkeys.
In sum, studies on alarm calling behavior need to take into account how a species’ ecology and social organization constrain individuals in how they can maximize their inclusive fitness. Predation is one of the most important evolutionary forces and continues to exert selection pressure on animal behavior. Across species, future studies should consider the relative potential contribution of individual, kin, and sexual selection on the evolution of alarm calling behavior.
Finally, alarm calling has long been thought as cognitively simple, the result of basic stimulus (predatory event)–response (alarm call) arithmetic. But new evidence across a range of species shows that behavioral decisions during predation can be cognitively complex, with signalers taking contextual information into account and producing alarm calling flexibly to maximize their benefits. In primates, receivers can infer complex information from calls by integrating pragmatic cues and social variables, suggesting that alarm calling reflects a species’ cognitive capacities as well as any other type of social behavior.
- Curio, E. (1978). The adaptive significance of avian mobbing. I. Teleonomic hypotheses and predictions. Zeitschrift für Tierpsychologie, 48, 175–183.Google Scholar
- Sperber, D. & Wilson, D. (1986). Relevance: Communication and cognition. Oxford: Blackwell.Google Scholar
- Stephan, C., & Zuberbühler, K. (2016). Persistent females and compliant males coordinate alarm calling in Diana monkeys. Current Biology, 26(21), 2907–2912.Google Scholar
- Zuberbühler, K. (2002). Effects of natural and sexual selection on the evolution of guenon loud calls. In M. E. Glenn & M. Cords (Eds.), The guenons: Diversity and adaptation in African monkeys (pp. 289–306). New York: Plenum.Google Scholar