Alarm signal

Some scientists have used the evidence of alarm-calling behaviour to challenge the theory that "evolution works only/primarily at the level of the gene and of the gene's "interest" in passing itself along to future generations." If alarm-calling is truly an example of altruism, then our understanding of natural selection becomes more complicated than simply "survival of the fittest gene".

Other researchers, generally those who support the selfish gene theory, question the authenticity of this "altruistic" behaviour. For instance, it has been observed that vervets sometimes emit calls in the presence of a predator, and sometimes do not. Studies show that these vervets may call more often when they are surrounded by their own offspring and by other relatives who share many of their genes.[5] Other researchers have shown that some forms of alarm calling, for example, "aerial predator whistles" produced by Belding's ground squirrels, do not increase the chances that a caller will get eaten by a predator; the alarm call is advantageous to both caller and recipient by frightening and warding off the predator.

Another theory suggests that alarm signals function to attract further predators, which fight over the prey organism, giving it a better chance of escape.[6] Others still suggest they are a deterrent to predators, communicating the animals alertness to the predator. One such case is the western swamphen (Porphyrio porphyrio), which gives conspicuous visual tail flicks (see also aposematism, handicap principle and stotting).[7]

Considerable research effort continues to be directed toward the purpose and ramifications of alarm-calling behaviour, because, to the extent that this research has the ability to comment on the occurrence or non-occurrence of altruistic behaviour, we can apply these findings to our understanding of altruism in human behaviour.

Vervet monkeys are the typical example of both animal alarm calls and of semantic capacity in non-human animals. They have three distinct calls for leopards, snakes, and eagles, and research shows that each call elicits different responses. When vervets are on the ground they respond to the eagle alarm call by looking up and running to cover, to leopard alarm calls primarily by looking up and running into a tree, and to the snake alarm call primarily by looking down. When in trees, vervets responded to the eagle alarm call by looking up and down and running out of trees, to the leopard alarm call by running higher in the tree and looking both up and down, and to the snake alarm call by looking primarily down.[8][9]

Each predator-specific behaviour is likely suited to escaping that predator, and, therefore, use of these escape behaviours is adaptive.[10]

Predator-specific alarm calls are an example of how monkeys organize a continuum of stimuli into categories that are judged to be more similar, and therefore belong to the same predator, or more different, and therefore belong to different predators.[10]

Campbell's mona monkeys also generate alarm calls, but in a different way than vervet monkeys. Instead of having discrete calls for each predator, Campbell monkeys have two distinct types of calls which contain different calls which consist in an acoustic continuum of affixes which change meaning. It has been suggested that this is a homology to human morphology.[11] Similarly, the cotton-top tamarin is able to use a limited vocal range of alarm calls to distinguish between aerial and land predators.[12] Both the Campbell monkey and the cotton-top tamarin have demonstrated abilities similar to vervet monkeys' ability to distinguish likely direction of predation and appropriate responses.[13][14]

That these three species use vocalizations to warn others of danger has been called by some proof of proto-language in primates. However, there is some evidence that this behavior does not refer to the predators themselves but to threat, distinguishing calls from words.[15]

Another species that exhibits alarm calls is the Barbary macaque. Barbary macaque mothers are able to recognize their own offspring's calls and behave accordingly.[16]

Diana monkeys produce alarm calls that differ based on caller, threat type, and habitat.

Diana monkeys also produce alarm signals. Adult males respond to each other's calls, showing that calling can be contagious.[17] Their calls differ based on signaller sex, threat type, habitat, and caller ontogenetic or lifetime predator experience.

Diana monkeys emit different alarm calls as a result of their sex. Male alarm calls are primarily used for resource defence, male–male competition, and communication between groups of conspecifics.[18] Female alarm calls are mainly used for communication within groups of conspecifics to avoid predation.[19]

Alarm calls are also predator-specific. In Taï National Park, Côte d'Ivoire, Diana monkeys are preyed on by leopards, eagles, and chimpanzees, but only emit alarm calls for leopards and eagles.[17][20] When threatened by chimpanzees, they use silent, cryptic behaviour and when threatened by leopards or eagles, they emit predator-specific alarm signals.[20] When researchers play recordings of alarm calls produced by chimpanzees in response to predation by leopards, about fifty per cent of nearby Diana monkeys switch from a chimpanzee antipredator response to a leopard antipredator response.[20] The tendency to switch responses is especially prominent among Diana monkey populations that live within the main range of the chimpanzee community.[20] This shift in antipredator response suggests that the monkeys interpret chimpanzee-produced, leopard-induced alarm calls as evidence for the presence of a leopard.[20] When the same monkeys are then played recordings of leopard growls, their reactions confirm that they had anticipated the presence of a leopard.[20] There are three possible cognitive mechanisms explaining how Diana monkeys recognize chimpanzee-produced, leopard-induced alarm calls as evidence for a nearby leopard: associative learning, causal reasoning, or a specialized learning programme driven by adaptive antipredator behaviour necessary for survival.[20]

In Taï National Park and Tiwai Island, Sierra Leone, specific acoustic markers in the alarm calls of Diana monkeys convey both threat type and caller familiarity information to a receiver. In Taï National Park, males respond to eagle alarm signals based on predator type and caller familiarity. When the caller is unfamiliar to the receiver, the response call is a 'standard' eagle alarm call, characterized by a lack of frequency transition at the onset of the call.[17] When the caller is familiar, the response call is an atypical eagle alarm call, characterized by a frequency transition at onset, and the response is faster than to that of unfamiliar caller.[17] On Tiwai Island, males respond in the opposite way to eagle alarm signals.[17] When the caller is familiar, the response call is a 'standard' eagle alarm call, without a frequency transition at onset. When the caller is unfamiliar, the response call is an atypical eagle alarm call, with a frequency transition at onset.[17]

The differences in alarm call responses are due to differences in habitat. In Taï National Park, there is a low predation risk from eagles, high primate abundance, strong intergroup competition, and a tendency for group encounters to result in high levels of aggression.[17] Therefore, even familiar males are a threat to whom males respond with aggression and an atypical eagle alarm call.[17] Only unfamiliar males, who are likely to be solitary and non-threatening, do not receive an aggressive response and receive only a typical alarm call.[17] On Tiwai Island, there is a high predation risk from eagles, low primate abundance, a tendency for group encounters to result in peaceful retreats, low resource competition, and frequent sharing of foraging areas.[17] Therefore, there is a lack of aggression towards familiar conspecifics to whom receivers respond with a 'standard' eagle call.[17] There is only aggression towards unfamiliar conspecifics, to whom receivers respond with an atypical call.[17] Simply put, a response with a typical eagle alarm call prioritizes the risk of predation, while a response with an atypical alarm call prioritizes social aggression.[17]

Diana monkeys also display a predisposition for flexibility in acoustic variation of alarm call assembly related to caller ontogenetic or lifetime predator experience. In Taï National Park and on Tiwai Island, monkeys have a predisposition to threat-specific alarm signals.[21] In Taï National Park, males produce three threat-specific calls in response to three threats: eagles, leopards, and general disturbances.[21] On Tiwai Island, males produce two threat-specific calls in response to two groups of threats: eagles, and leopards or general disturbances.[21] The latter are likely grouped together because leopards have not been present on the island for at least 30 years.[21] Other primates, such as Guereza monkeys and putty-nosed monkeys, also have two main predator-specific assemblies of alarm calls.[21][22][23] Predator-specific alarm signals differ based on call sequence assembly. General disturbances in Taï National Park and both general disturbances and leopards on Tiwai Island result in alarm calls assembled into long sequences.[21] Conversely, leopards in Taï National Park result in alarm calls that typically begin with voiced inhalations followed by a small number of calls.[21] These differences in alarm call arrangement between habitats are due to ontogenetic experience; specifically, a lack of experience with leopards on Tiwai Island causes them to be classified in the same predator category as general disturbances, and accordingly, leopards receive the same type of alarm call arrangement.[21]

In guenons, selection is responsible for the evolution of predator-specific alarm calls from loud calls. Loud calls travel long distances, greater than that of the home range, and can be used as beneficial alarm calls to warn conspecifics or showcase their awareness of and deter a predator.[24][25][26] A spectrogram of a subadult male call shows that the call is a composition of elements from a female alarm call and male loud call, suggesting the transition from the latter to the former during puberty and suggesting that alarm calls gave rise to loud calls through sexual selection.[26] Evidence of sexual selection in loud calls includes structural adaptations for long-range communication, co-incidence of loud calls and sexual maturity, and sexual dimorphism in loud calls.[26]

Not all scholars of animal communication accept the interpretation of alarm signals in monkeys as having semantic properties or transmitting "information". Prominent spokespersons for this opposing view are Michael Owren and Drew Rendall,[27][28] whose work on this topic has been widely cited and debated.[29][30] The alternative to the semantic interpretation of monkey alarm signals as suggested in the cited works is that animal communication is primarily a matter of influence rather than information, and that vocal alarm signals are essentially emotional expressions influencing the animals that hear them. In this view monkeys do not designate predators by naming them, but may react with different degrees of vocal alarm depending on the nature of the predator and its nearness on detection, as well as by producing different types of vocalization under the influence of the monkey's state and movement during the different types of escape required by different predators. Other monkeys may learn to use these emotional cues along with the escape behaviour of the alarm signaller to help make a good decision about the best escape route for themselves, without there having been any naming of predators.

Alarm signalling varies depending on the receiver's knowledge of a certain threat. Chimpanzees are significantly more likely to produce an alarm call when conspecifics are unaware of a potential threat or were not nearby when a previous alarm call was emitted.[33] Interestingly, when judging if conspecifics are unaware of potential dangers, chimpanzees do not solely look for behavioural cues, but also assess receiver mental states and use this information to target signalling and monitoring.[34] In a recent experiment, caller chimpanzees were shown a fake snake as a predator and were played pre-recorded calls from receivers. Some receivers emitted calls that were snake-related, and therefore represented receivers with knowledge of the predator, while other receivers emitted calls that were not snake-related, and therefore represented receivers without knowledge of the predator.[34] In response to the non-snake-related calls from receivers, the signallers increased their vocal and nonvocal signalling and coupled it with increased receiver monitoring.[34]

Chimpanzee age impacts the frequency of alarm signalling. Chimpanzees over 80 months of age are more likely to produce an alarm call than those less than 80 months of age.[35] There are several hypotheses for this lack of alarm calling in infants zero to four years of age.[35] The first hypothesis is a lack of motivation to produce alarm calls because of mothers in close proximity that minimize the infant's perception of a threat or that respond to a threat before the infant can.[35] Infants may also be more likely to use distress calls to catch their mother's attention in order for her to produce an alarm call.[35] Infants might also lack the physical ability to produce alarm calls or lack the necessary experience to classify unfamiliar objects as dangerous and worthy of an alarm signal.[35] Therefore, alarm calling may require advanced levels of development, perception, categorization, and social cognition.[35]

Other factors, such as signaller arousal, receiver identity, or increased risk of predation from calling, do not have a significant effect on the frequency of alarm call production.[33][34]

However, while alarm signals can be coupled with receiver monitoring, there is a lack of consensus on the definition, starting age, and purpose of monitoring. It is either defined as the use of three subsequent gaze alternations, from a threat to a nearby conspecific and back to the threat, or as the use of two gaze alternations.[35] Moreover, while some studies only report gaze alternation as starting in late juveniles, other studies report gaze alternation in infants as early as five months of age.[35] In infants and juveniles, it is potentially a means of social referencing or social learning through which younger chimpanzees check the reactions of more experienced conspecifics in order to learn about new situations, such as potential threats.[35] It has also been proposed to be a communicative behaviour or simply the result of shifts in attention between different environmental elements.[32][35]

The evolution of hominoid communication is evident through chimpanzee 'hoo' vocalizations and alarm calls. Researchers propose that communication evolved as natural selection diversified 'hoo' vocalizations into context-dependent 'hoos' for travel, rest, and threats.[36] Context-dependent communication is beneficial and likely maintained by selection as it facilities cooperative activities and social cohesion between signallers and receivers that can increase the likelihood of survival.[36] Alarm calls in chimpanzees also point to the evolution of hominoid language. Callers assess conspecifics' knowledge of threats, fill their need for information, and, in doing so, use social cues and intentionality to inform communication.[32][34] Filling a gap in information and incorporating social cues and intentionality into communication are all components of human language.[32][34] These shared elements between chimpanzee and human communication suggest an evolutionary basis, most likely that our last common ancestor with chimpanzees also possessed these linguistic abilities.[32][34][37]