Attention to elders' voice in non-human primates

The observed respect and attention to elders'' speech in traditional cultures appears to have a ‘universal’ component which questions its possible biological bases. Animals present differential attention to the vocalizations of other individuals according to their characteristics but little is known about the potential propensity to pay more attention to vocalizations of elders. On the basis of several hundreds of vocal exchanges recorded, here we show that aged female Campbell''s monkeys (Cercopithecus campbelli), despite being significantly less ‘loquacious’ than their younger adult counterparts, elicit many more responses when calling. These findings show that attention to elders'' vocal production appears in non-human primates, leading to new lines of questioning on human culture and language evolution.     

Campbell's Monkeys Use Affixation to Alter Call Meaning

Human language has evolved on a biological substrate with phylogenetic roots deep in the primate lineage. Here, we describe a functional analogy to a common morphological process in human speech, affixation, in the alarm calls of free-ranging adult Campbell''s monkeys (Cercopithecus campbelli campbelli). We found that male alarm calls are composed of an acoustically variable stem, which can be followed by an acoustically invariable suffix. Using long-term observations and predator simulation experiments, we show that suffixation in this species functions to broaden the calls'' meaning by transforming a highly specific eagle alarm to a general arboreal disturbance call or by transforming a highly specific leopard alarm call to a general alert call. We concluded that, when referring to specific external events, non-human primates can generate meaningful acoustic variation during call production that is functionally equivalent to suffixation in human language.     

Referential labelling in Diana monkeys

Animal semantic communication has received considerable theoretical and empirical attention because of its relevance to human language. Advances have been made by studies of alarm-call behaviour in nonhumans. In monkeys, for example, there is evidence that recipients have a fairly sophisticated understanding of a call's meaning; that is, the predator type usually associated with a certain alarm call. Little is known, however, about the mental mechanisms that drive call production in nonhuman primates. In some nonprimate species, it has been found that signallers do not respond to a predator's physical features but instead seem to respond to its relative threat or direction of attack. In these species, therefore, alarm calls do not denote different predator categories but simply reflect different types or levels of danger. Because different predator categories typically impose different types and degrees of threat it is entirely possible that nonhuman primates also respond to threat rather than a predator's category. This study examined how wild Diana monkeys, Cercopithecus diana, of the Ta? forest, Ivory Coast, label predation events. By altering playback stimuli and the position of a concealed speaker, I investigated whether Diana monkeys respond with acoustically different alarm calls depending on a predator's (1) distance (close versus far), (2) elevation (above versus below), or (3) category (eagle versus leopard). Analysis of male and female alarm-call behaviour showed that Diana monkeys consistently responded to predator category regardless of immediate threat or direction of attack. Data further suggested that, in addition to predator category, monkeys' alarm calls might also convey information about the predator's distance. Copyright 2000 The Association for the Study of Animal Behaviour.     

Use of male blue monkey “Pyow” calls for long-term individual identification

This study examines whether individual adult male blue monkeys (Cercopithecus mitis stuhlmanni) can be identified through acoustic analysis of their “pyow” calls. It is possible to reliably assign the pyow call of the blue monkeys of Kibale Forest, Uganda, to the individual caller based on the acoustic properties of the vocalization. Analysis of pyows made by a recognizable male over a 10-yr period shows that the acoustic properties of one individual's pyow call can remain relatively constant over time. Acoustic analysis of pyow calls may provide a relatively easy and reliable method to document tenure lengths of adult male blue monkeys resident in groups. Similar analyses of the loud calls of other species of primates may, likewise, prove to be useful in documenting long-term membership. © 1992 Wiley-Liss, Inc.     

Why do shrews twitter? Communication or simple echo-based orientation

Shrews are very vocal animals. We tested behaviourally whether the high-pitched laryngeal ‘twittering’ calls of as-yet unclear function serve for communication or echo-based orientation. We used a representative species from each of the two largest phylogenetic groups of shrews. In both species, experimental manipulation of substrate density, but not of the likelihood of conspecific presence, affected the shrews'' call rate when exploring an unknown environment. This adaptation of call rate to the degree of habitat clutter parallels bat echolocation and suggests that shrews may use the echoes and reverberations of their calls for identifying routes through their habitat or for probing habitat type. To assess the acoustic feasibility of shrew echo orientation, we ensonified shrew habitats in the field with an ‘artificial shrew’ (small speaker mounted close to a sensitive microphone). The data showed that shrew-like calls can indeed yield echo scenes useful for habitat assessment at close range, but beyond the range of the shrews'' vibrissae.     

Interspecies semantic communication in two forest primates

West African Diana monkeys (Cercopithecus diana) and Campbell's monkeys (Cercopithecus campbelli) frequently form mixed-species associations. Males of both species produce acoustically distinct alarm calls to crowned eagles (Stephanoaetus coronalus) and leopards (Panthera pardus), two of their main predators. Field playback experiments were conducted to investigate whether Diana monkeys respond to Campbell's alarm calls and whether they understand the calls' semantic content. Diana monkeys responded to playback of Campbell's leopard or eagle alarm calls as though the original predator were present. In a second experiment, Diana monkeys were primed with either Campbell's eagle or leopard alarm calls and then subsequently probed with the vocalizations of a crowned eagle or a leopard. Results showed that monkeys used the semantic information conveyed by the Campbell's alarm calls to predict the presence of a predator. The data are consistent with the hypothesis that non-human primates are able to use acoustic signals of diverse origin as labels for underlying mental representations.     

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.     

Predation increases acoustic complexity in primate alarm calls

According to most accounts, alarm calling in non-human primates is a biologically hardwired behaviour with signallers having little control over the acoustic structure of their calls. In this study, we compared the alarm calling behaviour of two adjacent populations of Diana monkeys at Taï forest (Ivory Coast) and Tiwai Island (Sierra Leone), which differ significantly in predation pressure. At Taï, monkeys regularly interact with two major predators, crowned eagles and leopards, while at Tiwai, monkeys are only hunted by crowned eagles. We monitored the alarm call responses of adult male Diana monkeys to acoustic predator models. We found no site-specific differences in the types of calls given to eagles, leopards and general disturbances, but there were consistent differences in how callers assembled calls into sequences. At Tiwai, males responded to leopards and general disturbances in the same way, while at Taï, males discriminated by giving call sequences that differed in the number of component calls. Responses to eagles were identical at both sites. We concluded that Diana monkeys are predisposed to use their repertoire in context-specific ways, but that ontogenetic experience determines how individual calls are assembled into meaningful sequences.     

The function of nonlinear phenomena in meerkat alarm calls

Nonlinear vocal phenomena are a ubiquitous feature of human and non-human animal vocalizations. Although we understand how these complex acoustic intrusions are generated, it is not clear whether they function adaptively for the animals producing them. One explanation is that nonlinearities make calls more unpredictable, increasing behavioural responses and ultimately reducing the chances of habituation to these call types. Meerkats (Suricata suricatta) exhibit nonlinear subharmonics in their predator alarm calls. We specifically tested the ‘unpredictability hypothesis’ by playing back naturally occurring nonlinear and linear medium-urgency alarm call bouts. Results indicate that subjects responded more strongly and foraged less after hearing nonlinear alarm calls. We argue that these findings support the unpredictability hypothesis and suggest this is the first study in animals or humans to show that nonlinear vocal phenomena function adaptively.     

Convergence and divergence in Diana monkey vocalizations

Individually distinct vocalizations are widespread among social animals, presumably caused by variation in vocal tract anatomy. A less-explored source of individual variation is due to learned movement patterns of the vocal tract, which can lead to vocal convergence or divergence in social groups. We studied patterns of acoustic similarity in a social call produced by 14 female Diana monkeys (Cercopithecus diana) in two free-ranging groups. Calls showed variability in fundamental frequency contours owing to individual identity and external context. Vocal divergence increased significantly between females during poor visibility and tended to increase in the presence of neighbours. In contrast, vocal convergence increased significantly between females during vocal interactions, because females matched the frequency contour of their own call with another female's preceding call. Our findings demonstrate that these primates have some control over the acoustic fine structure of their most important social vocalization. Vocal convergence and divergence are two opposing processes that enable callers to ensure spatial proximity and social cohesion with other group members.     

Monkeys crying wolf? Tufted capuchin monkeys use anti-predator calls to usurp resources from conspecifics

The use of ‘tactical deception’ is argued to have been important in the cognitive evolution of the order Primates, but systematic studies of active deception in wild non-human primates are scant. This study tests whether wild tufted capuchin monkeys (Cebus apella nigritus) use alarm calls in a functionally deceptive manner to usurp food resources. If capuchins use alarm calls ‘deceptively’, it was predicted that false alarms should be: (i) given by subordinates more than by dominants, (ii) more frequent when food is most contestable, (iii) more frequent when less food is available, and (iv) given when the caller is in a spatial position in which it could increase its feeding success if conspecifics react to the call. These predictions were tested by observing subjects in experimental contexts, in which the amount and distribution of a high-value resource (banana pieces) were manipulated using wooden platforms suspended from tree branches. While false alarms were non-significantly more common when more food was available, the three remaining predictions were supported. These results generally support the hypothesis that alarm calls are used by capuchins to reduce the effects of feeding competition. Whether this is intentional on the part of the caller requires further investigation.     

Breaking the trade-off: rainforest bats maximize bandwidth and repetition rate of echolocation calls as they approach prey

Both mammals and birds experience a performance trade-off between producing vocalizations with high bandwidths and at high repetition rate. Echolocating bats drastically increase repetition rate from 2–20 calls s⁻¹ up to about 170 calls s⁻¹ prior to intercepting airborne prey in order to accurately track prey movement. In turn, bandwidth drops to about 10–30 kHz for the calls of this ‘final buzz’. We have now discovered that Southeast Asian rainforest bats (in the vespertilionid subfamilies Kerivoulinae and Murininae) are able to maintain high call bandwidths at very high repetition rates throughout approach to prey. Five species of Kerivoula and Phoniscus produced call bandwidths of between 78 and 170 kHz at repetition rates of 140–200 calls s⁻¹ and two of Murina at 80 calls s⁻¹. The ‘typical’ and distinct drop in call frequency was present in none of the seven species. This stands in striking contrast to our present view of echolocation during approach to prey in insectivorous bats, which was established largely based on European and American members of the same bat family, the Vespertilionidae. Buzz calls of Kerivoula pellucida had mean bandwidths of 170 kHz and attained maximum starting frequencies of 250 kHz which makes them the most broadband and most highly pitched tonal animal vocalization known to date. We suggest that the extreme vocal performance of the Kerivoulinae and Murininae evolved as an adaptation to echolocating and tracking arthropods in the dense rainforest understorey.     

Noise-Induced Frequency Modifications of Tamarin Vocalizations: Implications for Noise Compensation in Nonhuman Primates

Previous research suggests that nonhuman primates have limited flexibility in the frequency content of their vocalizations, particularly when compared to human speech. Consistent with this notion, several nonhuman primate species have demonstrated noise-induced changes in call amplitude and duration, with no evidence of changes to spectral content. This experiment used broad- and narrow-band noise playbacks to investigate the vocal control of two call types produced by cotton-top tamarins (Saguinus Oedipus). In ‘combination long calls’ (CLCs), peak fundamental frequency and the distribution of energy between low and high frequency harmonics (spectral tilt) changed in response to increased noise amplitude and bandwidth. In chirps, peak and maximum components of the fundamental frequency increased with increasing noise level, with no changes to spectral tilt. Other modifications included the Lombard effect and increases in chirp duration. These results provide the first evidence for noise-induced frequency changes in nonhuman primate vocalizations and suggest that future investigations of vocal plasticity in primates should include spectral parameters.     

Grooming-at-a-distance by exchanging calls in non-human primates

The ‘social bonding hypothesis'' predicts that, in large social groups, functions of gestural grooming should be partially transferred to vocal interactions. Hence, vocal exchanges would have evolved in primates to play the role of grooming-at-a-distance in order to facilitate the maintenance of social cohesion. However, there are few empirical studies testing this hypothesis. To address this point, we compared the rate of contact call exchanges between females in two captive groups of Japanese macaques as a function of female age, dominance rank, genetic relatedness and social affinity measured by spatial proximity and grooming interactions. We found a significant positive relationship between the time spent on grooming by two females and the frequency with which they exchanged calls. Our results conform to the predictions of the social bonding hypothesis, i.e. vocal exchanges can be interpreted as grooming-at-a-distance.     

Age- and sex-specific patterns of vocal behavior in De Brazza's monkeys (Cercopithecus neglectus)

Although vocal production is strongly genetically determined in nonhuman primates, vocal usage is more likely to be influenced by experience. Nonetheless, sex differences in both production and usage can be found in the vocal repertoire of adults, but little attention has been paid to their ontogeny. Here, we provide the first comprehensive analysis of the vocal repertoire of De Brazza's monkeys (Cercopithecus neglectus), with particular attention to age- and sex-specific patterns. This species has special interest because it is the only monogamous species of guenons, but it nevertheless shares the strong sexual morphological and behavioral dimorphism seen in other guenons. A structurally based classification of calls recorded in 23 captive individuals has been cross-validated by an analysis of the associated contexts of emission. We identified sound units that could be uttered alone or concatenated to form 10 call types, including only three types shared by all age-sex-classes. Both age- and sex-discrepancy in terms of phonation could be explained by maturational changes and morphological dimorphism. In general, call production and usage parallel those seen in other guenons, suggesting that phylogeny and sexual dimorphism play important roles in vocal communication in this species. However, the boundary between adult male and female vocal repertoires appeared to be less strict than previously reported, suggesting that both sexes have the capacity to produce calls of the other sex but that social roles may constrain this expression. Similarly, age-specific vocal patterns would reflect respective social roles, and experience to some extent. Finally, calling rates would reflect age-/sex-specific degree of involvement in intragroup social networks. These findings highlight the relative importance of phylogeny, morphology, and social system on the shaping of individual repertoires in nonhuman primates.     

Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques

To date, there have been no investigations of the behavioral effects of interleukin-1 (IL-1) in nonhuman primates. In this study the locomotor behavior and vocalizations of juvenile rhesus monkeys were monitored for 45 minutes following intravenous injections of recombinant human IL-1 alpha. In addition, their reaction to a broadcasted recording of infant monkey distress calls was determined 20 minutes after the beginning of each test session. IL-1 induced sleep-like inactivity and significantly diminished the monkey's behavioral and vocal responses to the broadcasted calls. The coo calls uttered by the monkeys following IL-1 treatment also had a longer duration and lower fundamental frequency than calls during the control condition. As several studies have indicated that behavioral effects of IL-1 may be mediated by corticotropin-releasing hormone (CRH), a second group of rhesus monkeys was given injections of CRH. CRH did not alter behavior or call structure at the dose administered. These results extend previous research on the behavioral effects of IL-1 to include the nonhuman primate and provide the first evidence that cytokines can affect vocal communication in rhesus monkeys. © 1995 Wiley-Liss, Inc.     

Divergence of Acoustic Signals in a Widely Distributed Frog: Relevance of Inter-Male Interactions

Divergence of acoustic signals in a geographic scale results from diverse evolutionary forces acting in parallel and affecting directly inter-male vocal interactions among disjunct populations. Pleurodema thaul is a frog having an extensive latitudinal distribution in Chile along which males'' advertisement calls exhibit an important variation. Using the playback paradigm we studied the evoked vocal responses of males of three populations of P. thaul in Chile, from northern, central and southern distribution. In each population, males were stimulated with standard synthetic calls having the acoustic structure of local and foreign populations. Males of both northern and central populations displayed strong vocal responses when were confronted with the synthetic call of their own populations, giving weaker responses to the call of the southern population. The southern population gave stronger responses to calls of the northern population than to the local call. Furthermore, males in all populations were stimulated with synthetic calls for which the dominant frequency, pulse rate and modulation depth were varied parametrically. Individuals from the northern and central populations gave lower responses to a synthetic call devoid of amplitude modulation relative to stimuli containing modulation depths between 30–100%, whereas the southern population responded similarly to all stimuli in this series. Geographic variation in the evoked vocal responses of males of P. thaul underlines the importance of inter-male interactions in driving the divergence of the acoustic traits and contributes evidence for a role of intra-sexual selection in the evolution of the sound communication system of this anuran.     

Vervet monkey alarm calls: Semantic communication in a free-ranging primate

Vervet monkeys (Cercopithecus aethiops) at Amboseli, Kenya, give acoustically different alarm calls to different predators. Each alarm evokes contrasting, seemingly adaptive, responses. Animals on the ground respond to leopard alarms by running into trees, to eagle alarms by looking up, and to snake alarms by looking down. In a 14-month field study examining the semantic properties of alarm calls, we played tape-recorded alarms to vervets in the absence of actual predators and filmed the monkeys' responses. Playbacks confirmed observations and showed that (1) alarm length, amplitude and alarmist's age/sex class had little effect on response quality, and (2) context was not a systematic determinant of response. We conclude that vervet alarm calls function to designate different classes of external danger.     

Hearing and communication in blue monkeys (Cercopithecus mitis)

Hearing and vocal communication in blue monkeys (Cercopithecus mitis) was studied within an ecological context. Field measurements of the acoustical characteristics of the blue monkey's natural habitat were conducted in the Kibale forest (Uganda) and in Kakamega forest (Kenya). Measurements of background noise levels indicated that vocal communication pitched in the 100–1000-Hz frequency band would be relatively unimpeded by disruptive background noises. Furthermore, measurements of the propagation rate of audio signals indicated that calls pitched in the 125–200-Hz region penetrated the forest with minimal decrement in amplitude. Tests of the blue monkey's acoustic sensitivyty and range of hearing were conducted in the laboratory with standard audiometric procedures. Hearing in the blue monkey was characterized by a U-shaped function, with maximum sensitivity of about 5 dB SPL spanning a four-octave range from 1 to 16 kHz. The hearing of blue monkeys was superior to human hearing for tones below 500 Hz and above 8 kHz in frequency. A comparative analysis of primate hearing indicated that the blue monkey was approximately 18 dB more sensitive to low-frequency tones than the comparably sized, semi-terrestrial rhesus monkey (Macaca mulatta). Furthermore, blue monkeys exhibit phonatory specializations for vocal production in this relatively unused, low-frequency band of 125–200 Hz. These specializations for low-frequency vocal production and low-frequency hearing collectively act to increase the effective distance of long-range acoustic communication in the forest canopy.     

‘Compromise’ in Echolocation Calls between Different Colonies of the Intermediate Leaf-Nosed Bat (Hipposideros larvatus)

Each animal population has its own acoustic signature which facilitates identification, communication and reproduction. The sonar signals of bats can convey social information, such as species identity and contextual information. The goal of this study was to determine whether bats adjust their echolocation call structures to mutually recognize and communicate when they encounter the bats from different colonies. We used the intermediate leaf-nosed bats (Hipposideros larvatus) as a case study to investigate the variations of echolocation calls when bats from one colony were introduced singly into the home cage of a new colony or two bats from different colonies were cohabitated together for one month. Our experiments showed that the single bat individual altered its peak frequency of echolocation calls to approach the call of new colony members and two bats from different colonies adjusted their call frequencies toward each other to a similar frequency after being chronically cohabitated. These results indicate that the ‘compromise’ in echolocation calls might be used to ensure effective mutual communication among bats.