Klaus Zuberbühler

Diana monkey long-distance calls: Messages for conspecifics and predators

Abstract Primate long-distance calls have typically been interpreted as communication signals between conspecific groups (the ‘resource defence hypothesis’), but their potential role as anti-predator alarm calls has received comparably little attention. Male diana monkeys,Cercopithecus diana dianain the Tai forest of Cote d’Ivoire often utter long-distance calls, either spontaneously or in reaction to a variety of stimuli, including predators and non-predators. The present study focuses only on predation contexts and provides evidence for communication to both predators and conspecifics. Males called only in response to predators whose hunting success depends on unprepared prey, that is, leopards and crowned hawk eagles, but not in response to pursuit hunters, such as chimpanzees and humans, which can pursue the caller in the canopy. Calling was regularly combined with approaching the predator. Both observations suggest that male long-distance calls are used to signal detection to the predator (‘perception advertisement hypothesis’). Analysis of male long-distance calls given to leopards and eagles showed that they differed according to a number of acoustic parameters. The two call variants were played to different diana monkey groups; conspecifics responded to them as though the original predator were present. We conclude that, in addition to their function in perception advertisement, diana monkey long-distance calls function as within-group semantic signals that denote different types of predators.

Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution

Fossils and molecular data are two independent sources of information that should in principle provide consistent inferences of when evolutionary lineages diverged. Here we use an alternative approach to genetic inference of species split times in recent human and ape evolution that is independent of the fossil record. We first use genetic parentage information on a large number of wild chimpanzees and mountain gorillas to directly infer their average generation times. We then compare these generation time estimates with those of humans and apply recent estimates of the human mutation rate per generation to derive estimates of split times of great apes and humans that are independent of fossil calibration. We date the human–chimpanzee split to at least 7–8 million years and the population split between Neanderthals and modern humans to 400,000–800,000 y ago. This suggests that molecular divergence dates may not be in conflict with the attribution of 6- to 7-million-y-old fossils to the human lineage and 400,000-y-old fossils to the Neanderthal lineage.

Chimpanzees modify recruitment screams as a function of audience composition

Wild chimpanzees produce acoustically distinct scream vocalizations depending on their social role during agonistic interactions with other group members. Here, we show that victims during such agonistic interactions alter the acoustic structure of their screams depending on the severity of aggression experienced, providing nearby listeners with important cues about the nature of the attack. However, we also found that victims of severe attacks produced screams that significantly exaggerated the true level of aggression experienced, but they did so only if there was at least one listener in the audience who matched or surpassed the aggressor in rank. Our results are consistent with the more general hypothesis that chimpanzees possess sophisticated understanding of third-party relationships, so-called triadic awareness, and that this knowledge influences their vocal production.

Campbell's monkeys concatenate vocalizations into context-specific call sequences

Primate vocal behavior is often considered irrelevant in modeling human language evolution, mainly because of the callers limited vocal control and apparent lack of intentional signaling. Here, we present the results of a long-term study on Campbells monkeys, which has revealed an unrivaled degree of vocal complexity. Adult males produced six different loud call types, which they combined into various sequences in highly context-specific ways. We found stereotyped sequences that were strongly associated with cohesion and travel, falling trees, neighboring groups, nonpredatory animals, unspecific predatory threat, and specific predator classes. Within the responses to predators, we found that crowned eagles triggered four and leopards three different sequences, depending on how the caller learned about their presence. Callers followed a number of principles when concatenating sequences, such as nonrandom transition probabilities of call types, addition of specific calls into an existing sequence to form a different one, or recombination of two sequences to form a third one. We conclude that these primates have overcome some of the constraints of limited vocal control by combinatorial organization. As the different sequences were so tightly linked to specific external events, the Campbells monkey call system may be the most complex example of ‘proto-syntax’ in animal communication known to date.

A syntactic rule in forest monkey communication

Abstract Syntactic rules allow a speaker to combine signals with existing meanings to create an infinite number of new meanings. Even though combinatory rules have also been found in some animal communication systems, they have never been clearly linked to concurrent changes in meaning. The present field experiment indicates that wild Diana monkeys, Cercopithecus diana, may comprehend the semantic changes caused by a combinatory rule present in the natural communication of another primate, the Campbells monkey, C. campbelli. Campbells males give acoustically distinct alarm calls to leopards, Panthera pardus, and crowned-hawk eagles, Stephanoaetus coronatus, and Diana monkeys respond to these calls with their own corresponding alarm calls. However, in less dangerous situations, Campbells males emit a pair of low, resounding ‘boom’ calls before their alarm calls. Playbacks of boom-introduced Campbells alarm calls no longer elicited alarm calls in Diana monkeys, indicating that the booms have affected the semantic specificity of the subsequent alarm calls. When the booms preceded the alarm calls of Diana monkeys, however, they were no longer effective as semantic modifiers, indicating that they are meaningful only in conjunction with Campbells alarm calls. I discuss the implications of these findings for the evolution of syntactic abilities.

Urinary oxytocin and social bonding in related and unrelated wild chimpanzees

Animals that maintain cooperative relationships show gains in longevity and offspring survival. However, little is known about the cognitive or hormonal mechanisms involved in cooperation. Indeed, there is little support for a main hypothesis that non-human animals have the cognitive capacities required for bookkeeping of cooperative exchanges. We tested an alternative hypothesis that cooperative relationships are facilitated by an endocrinological mechanism involving oxytocin, a hormone required for bonding in parental and sexual relationships across mammals. We measured urinary oxytocin after single bouts of grooming in wild chimpanzees. Oxytocin levels were higher after grooming with bond partners compared with non-bond partners or after no grooming, regardless of genetic relatedness or sexual interest. We ruled out other possible confounds, such as grooming duration, grooming direction or sampling regime issues, indicating that changes in oxytocin levels were mediated by social bond strength. Oxytocin, which is thought to act directly on neural reward and social memory systems, is likely to play a key role in keeping track of social interactions with multiple individuals over time. The evolutionary linkage of an ancestral hormonal system with complex social cognition may be the primary mechanism through which long-term cooperative relationships develop between both kin and non-kin in mammals.

Predator-specific alarm calls in Campbell's monkeys, Cercopithecus campbelli

Abstract. One of the most prominent behavioural features of many forest primates are the loud calls given by the adult males. Early observational studies repeatedly postulated that these calls function in intragroup spacing or intergroup avoidance. More recent field experiments with Diana monkeys (Cercopithecus diana) of Taï Forest, Ivory Coast, have clearly shown that loud male calls function as predator alarm calls because calls reliably (1) label different predator classes and (2) convey semantic information about the predator type present. Here, I test the alarm call hypothesis another primate, the Campbells monkey (C. campbelli). Like Diana monkeys, male Campbells monkeys produce conspicuous loud calls to crowned hawk eagles (Stephanoaetus coronatus) and leopards (Panthera pardus), two of their main predators. Playback experiments showed that monkeys responded to the predator category represented by the different playback stimuli, regardless of whether they consisted of (1) vocalisations of the actual predators (crowned hawk eagle shrieks or leopard growls), (2) alarm calls to crowned hawk eagles or leopards given by other male Campbells monkeys or (3) alarm calls to crowned hawk eagles or leopards given by sympatric male Diana monkeys. These experiments provide further evidence that non-human primates have evolved the cognitive capacity to produce and respond to referential labels for external events.

Hornbills can distinguish between primate alarm calls.

Some mammals distinguish between and respond appropriately to the alarm calls of other mammal and bird species. However, the ability of birds to distinguish between mammal alarm calls has not been investigated. Diana monkeys (Cercopithecus diana) produce different alarm calls to two predators: crowned eagles (Stephanoaetus coronatus) and leopards (Panthera pardus). Yellow–casqued hornbills (Ceratogymna elata) are vulnerable to predation by crowned eagles but are not preyed on by leopards and might therefore be expected to respond to the Diana monkey eagle alarm call but not to the leopard alarm call. We compared responses of hornbills to playback of eagle shrieks, leopard growls, Diana monkey eagle alarm calls and Diana monkey leopard alarm calls and found that they distinguished appropriately between the two predator vocalizations as well as between the two Diana monkey alarm calls. We discuss possible mechanisms leading to these responses.

Lethal aggression in Pan is better explained by adaptive strategies than human impacts

Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fitness benefits by increasing their access to resources such as food or mates. Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning. To discriminate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n = 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 communities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive explanations for killing by chimpanzees, whereas the human impact hypothesis is not supported.

The central importance of information in studies of animal communication

The concept of information plays a central role in studies of animal communication. Animals’ responses to the calls of different individuals, to food calls, alarm calls, and to signals that predict behaviour, all suggest that recipients acquire information from signals and that this information affects their response. Some scientists, however, want to replace the concept of information with one based on the ‘manipulation’ of recipients by signallers through the induction of nervous-system responses. Here we review both theory and data that argue against hypotheses based exclusively on manipulation or on a fixed, obligatory link between a signal’s physical features and the responses it elicits. Results from dozens of studies indicate that calls with ‘arousing’ or ‘aversive’ features may also contain information that affects receivers’ responses; that acoustically similar calls can elicit different responses; acoustically different calls can elicit similar responses; and ‘eavesdropping’ animals respond to the relationship instantiated by signal sequences. Animal signals encode a surprisingly rich amount of information. The content of this information can be studied scientifically.