Functionally referential communication in a chimpanzee

The evolutionary origins of the use of speech signals to refer to events or objects in the world have remained obscure. Although functionally referential calls have been described in some monkey species, studies with our closest living relatives, the great apes, have not generated comparable findings. These negative results have been taken to suggest that ape vocalizations are not the product of their otherwise sophisticated mentality and that ape gestural communication is more informative for theories of language evolution. We tested whether chimpanzee rough grunts, which are produced during feeding contexts, functioned as referential signals. Individuals produced acoustically distinct types of "rough grunts" when encountering different foods. In a naturalistic playback experiment, a focal subject was able to use the information conveyed by these calls produced by several group mates to guide his search for food, demonstrating that the different grunt types were meaningful to him. This study provides experimental evidence that our closest living relatives can produce and understand functionally referential calls as part of their natural communication. We suggest that these findings give support to the vocal rather than gestural theories of language evolution.     

How vervet monkeys perceive their grunts: Field playback experiments

Free-ranging vervet monkeys grunt to each other in a variety of social situations: when approaching a dominant or subordinate individual, when moving into a new area of their range, or when observing another group. Like other non-human primate vocalizations, these grunts have traditionally been interpreted as a single, highly variable call that reflects the arousal state of the signaller. Field playback experiments suggest, however, that what humans initially perceive as one grunt the monkeys perceive as at least four. Each grunt carries a specific meaning that seems to depend more on its acoustic properties than on the context in which it occurs. Results suggest that the vocalizations given by monkeys during social interactions may function in a rudimentary representational manner, as if to designate objects or events in the external world.     

Selection for acoustic individuality within the vocal repertoire of wild chimpanzees

Individual primates typically produce acoustically distinct calls. To investigate the factors that facilitate the evolution of individual vocal signatures, we examined two components of the call repertoire of chimpanzees: the pant hoot and pant grunt. Pant hoots are long-distance signals whose recipients can be several hundred meters away, while pant grunts are short-range calls given to conspecifics within close visual range. Given their markedly different contexts of emission, we predicted that natural selection would favor the elaboration of individually distinctive acoustic features in pant hoots compared with pant grunts. Analyses of nine acoustic features revealed that pant hoots are more stereotyped within-individuals and variable between-individuals than pant grunts. These data are consistent with the hypothesis that selection may act to encode varying degrees of individuality in different components of the vocal repertoire of a single species.     

Factors Affecting Acoustic Variation in Barbary-macaque (Macaca sylvanus) Disturbance Calls

Semi-free-ranging Barbary macaques (Macaca sylvanus) were observed to utter distinctive calls after disturbances in the surroundings (e.g. presence of a predator, occurrence of some unusual phenomenon). These calls differed from calls given in other contexts. Most of these calls were uttered in a serial manner, some of which lasted as long as the corresponding context. The aim of this study was to determine the object-related specificity of calls and variation of acoustic parameters within a call series. The analysis revealed that acoustic features of calls varied among contexts. Within one apparently homogeneous context, both temporal and frequency characteristics shifted gradually. Furthermore, the disturbance calls clearly differed between individuals. To examine the disturbance calls' meaning, playback experiments were conducted in which alarm calls and disturbance calls were presented. After playback of an alarm call, subjects typically showed an escape response, whereas, in response to disturbance calls, they most often scanned the surroundings. Juvenile animals generally showed stronger responses than adults.     

Context-specific calls in wild chimpanzees, Pan troglodytes verus: analysis of barks

Context-specific calls, which have a distinct acoustic structure and are selectively produced in specific contexts, are a prerequisite for calls that function referentially. Functionally referential calls, which convey information to conspecifics about objects and events in the external world, have been found in a number of species, notably primates. Evidence of context-specific calls in apes, however, is largely absent. We analysed whether the barks of wild male chimpanzees in the Ta? Forest, Côte d'Ivoire, are context specific. We examined the acoustic structure of barks, and other calls produced in association with barks, in six contexts, using discriminant function analysis. Chimpanzees produced context-specific signals in two ways. First, they produced two acoustically graded bark subtypes, in hunt and snake contexts, respectively. Second, they produced context-specific signal combinations of barks with acoustically different call types or drums. These signal combinations increased specificity levels in three of the six contexts to over 90%, a level similar to the classic vervet monkey, Cercophithecus aethiops, predator alarm calls. Furthermore, specific chimpanzee signals were produced in contexts other than alarm, such as travel and hunting, where the potential benefits of evolving specific calls are less obvious. These signals may convey specific context information to listeners, and thus function referentially; however, to confirm this, analyses of listeners' responses are required. The results show that two strategies for producing context-specific signals seem to have evolved in a species other than humans: chimpanzees produce context-specific bark subtypes and context-specific signal combinations. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Production and perception of sex differences in vocalizations of Wied's black‐tufted‐ear marmosets (Callithrix kuhlii)

Males and females from many species produce distinct acoustic variations of functionally identical call types. Social behavior may be primed by sex‐specific variation in acoustic features of calls. We present a series of acoustic analyses and playback experiments as methods for investigating this subject. Acoustic parameters of phee calls produced by Wied's black‐tufted‐ear marmosets (Callithrix kuhlii) were analyzed for sex differences. Discriminant function analyses showed that calls contained sufficient acoustic variation to predict the sex of the caller. Several frequency variables differed significantly between the sexes. Natural and synthesized calls were presented to male–female pairs. Calls elicited differential behavioral responses based on the sex of the caller. Marmosets became significantly more vigilant following the playback of male phee calls (both natural and synthetic) than following female phee calls. In a second playback experiment, synthesized calls were modified by independently manipulating three parameters that were known to differ between the sexes (low‐, peak‐, and end‐frequency). When end‐frequency‐modified calls were presented, responsiveness was differentiable by sex of caller but did not differ from responses to natural calls. This suggests that marmosets did not use end‐frequency to determine the sex of the caller. Manipulation of peak‐and low‐frequency parameters eliminated the discrete behavioral responses to male and female calls. Together, these parameters may be important features that encode for the sex‐specific signal. Recognition of sex by acoustic cues seems to be a multivariate process that depends on the congruency of acoustic features. Am. J. Primatol. 71:324–332, 2009. © 2008 Wiley‐Liss, Inc.     

Playbacks of food-associated calls attract chimpanzees towards known food patches in a captive setting

Food-associated calls have received much research attention due to their potential to refer to discovered food in a word-like manner. Studies have found that in many species, food-associated calls attract receivers to the food patch, suggesting these calls play roles in food sharing, cooperation and competition. Additionally, in various species, these calls play a role that has received much less attention: mediating social interactions among foragers that are already nearby or within the food patch, independently of whether they attract outside foragers. In order to increase understanding of the function of the chimpanzee (Pan troglodytes) food-associated rough grunt, we conducted captive playback studies testing whether rough grunt playbacks attract, repel or have no effect on the proximity of foragers already familiarized with the presence of food. We tested how acoustic playbacks of rough grunts (or control calls) from one of two known, identical feeding sites affected receivers’ approach and feeding behaviors. More often than expected, participants first approached the feeding site from which rough grunts, but not control calls, were broadcast. However, neither condition increased the likelihood that participants fed first from a given site. Our results support the hypothesis that rough grunts elicit an approach response in receivers, while providing no evidence that they repel. In addition, our study provides evidence that receivers may approach rough grunts even if they do not intend to feed. We discuss the information rough grunts may convey to receivers beyond information about discovered food and the potential benefits signalers may gain from this calling behavior.

     

Alternative Male Spawning Tactics and Acoustic Signals in the Plainfin Midshipman Fish Porichthys notatus Girard (Teleostei,Batrachoididae)

The plainfin midshipman Porichthys notatus has two male reproductive morphs, ‘Type I’ and ‘Type II’, which are distinguishable by their physical traits alone. Type I males are eight times larger in body mass than Type II males and have a six-fold larger relative sonic (vocal) muscle mass than Type II males. In contrast, the testicles of Type II males are seven times larger than those of Type I males. This study demonstrates morph-specific patterns of reproduction, including acoustic signals, for Type I and II males. Field censuses of nests showed that only Type 1 males maintained nests. Type II males and females transiently appeared in these nests in association with each other. Infra-red video and hydrophone recordings in aquaria showed that Type I males maintained nests and readily vocalized. Long-duration ‘hums’ and sequences of short-duration ‘grunts’ were produced during advertisement and agonistic contexts, respectively. Humming Type I males attracted females to their nests, pair-spawned, and then guarded egg clutches alone. By contrast, Type II males neither acoustically courted females nor maintained available nest sites, but rather ‘sneak-’ or ‘satellite-spawned’ at the nests of Type I males. Type II males infrequently produced low amplitude, short duration grunts that were similar in spectral, temporal and amplitude characteristics to the grunts of females. Type II males appear to be obligate sexual parasites of the nest-building, mate-calling, and egg-guarding Type I males. The dimorphic body and vocal muscle traits of the two male morphs in the plainfin midshipman are thus paralleled by a divergence in their reproductive tactics and the properties of their acoustic signals.     

Responses to natural and synthetic phee calls by common marmosets (Callithrix jacchus)

Captive adult common marmosets (Callithrix jacchus) produce whistlelike “phee” calls in two contexts: in the home cage, where phee calls may function as part of territorial marking behavior, and when separated from social companions, where phee calls may function to reunite conspecifics. Natural and synthesized calls representing the acoustic structure of male and female calls in each context were presented to adult marmosets in a playback paradigm. Marmosets demonstrated discriminative abilities according to the context of the call and the caller's sex. Vocal and behavioral responses indicated increased vigilance and territorial behavior, following playbacks of naturally produced calls as well as synthetic calls. All animals scanned more frequently following produced calls as well as synthetic calls. All animals scanned more frequently following natural home cage as well as isolation calls, but only increased contact behavior (trills) in response to home cage calls. The responses were dimorphic according to the sex of the caller, where adult males scanned more following male calls, and adult females were more aggressive following male and female calls. The differential behavioral responses to playbacks of marmoset phee calls suggest a biological relevance to subtle differences found in the acoustic parameters of the phee call. © 1994 Wiley-Liss, Inc.

1 This article is a US Government work and, as such, in the public domain in the United States of America.

     

饲养状态真鲂(鱼弗)发声的昼夜与季节变化

本文研究了受水温和光周期等自然变化影响的饲养状态真鲂鮄发声的昼夜与季节变化,并研究了实验鱼活动(鱼类游泳次数)的日变化。声音信号的昼夜节律记录发声活动的日常水平(摄食之外的时期),但是每月变化的记录(季节性式型)则在摄食期间进行,因为摄食时声音信号增加,而日常发声活动较不频繁。实验鱼包括雌雄两性,且未达性成熟。真鲂鮄在白天发声多一些,也更活跃。声音为阵发式的,较不频繁(平均值=0.04发声/min每鱼每天)。最少的发声活动出现在晚上,凌晨和黄昏居中(声音的阵发更频繁,但是声音更少),最多的发声活动出现在白天(声音的阵发更频繁,并且含更多数目的声音)。竞争摄食时声音信号的比率不呈现季节性变化(平均值=3.98发声/min每鱼),与温度也不相关,显示出竞争摄食时声音的发出以最大比率进行。敲击声和呼噜声的某些声学特征与温度相关,特别是在较高的温度下呼噜声的节拍间隔急剧下降。敲击声和呼噜声的声音参数中的季节性变化,多数可以解释为发声肌肉和中央声音控制回路的温度效应。     

Acoustic characteristics and variations in grunt vocalizations in the oyster toadfish <Emphasis Type="Italic">Opsanus tau</Emphasis>

Acoustic communication is critical for reproductive success in the oyster toadfish Opsanus tau. While previous studies have examined the acoustic characteristics, behavioral context, geographical variation, and seasonality of advertisement boatwhistle sound production, there is limited information on the grunt or other non-advertisement vocalizations in this species. This study continuously monitored sound production in toadfish maintained in an outdoor habitat for four months to identify and characterize grunt vocalizations, compare them with boatwhistles, and test for relationships between the incidence of grunt vocalizations, sound characteristics and environmental parameters. Oyster toadfish produced grunts in response to handling, and spontaneous single (70% of all grunts), doublet (10%), and trains of grunts (20%) throughout the May to September study period. Grunt types varied in pulse structure, duration, and frequency components, and were shorter and of lower fundamental frequency than the pulse repetition rate of boatwhistles. Higher water temperatures were correlated with a greater number of grunt emissions, higher fundamental frequencies, and shorter sound durations. The number of grunts per day was also positively correlated with daylength and maximum tidal amplitude differences (previously entrained) associated with full and new moons, thus providing the first demonstration of semilunar vocalization rhythms in the oyster toadfish. These data provide new information on the acoustic repertoire and the environmental factors correlated with sound production in the toadfish, and have important implications for seasonal acoustic communication in this model vocal fish.     

Grunt to go—Vocal coordination of group movements in redfronted lemurs

To remain cohesive as a group, individuals must coordinate their movements between resources. In many species, vocalisations are used in this context. While some species have specific movement calls, others use calls which are also employed in different contexts. The use of such multicontextual calls has rarely been studied quantitatively, especially during both the pre‐departure and departure period associated with collective decisions. We thus investigated the use of close calls (“grunts”) for the coordination of collective movements in four groups of wild redfronted lemurs (Eulemur rufifrons) in Kirindy Forest, Western Madagascar. Group movements are started by an initiator, who moves away from the group and is joined by followers setting out in the same direction. We observed collective movements and recorded vocalisations from 18 focal individuals (54 movements recorded for followers, 21 for initiators). The grunt rate of both initiators and followers was higher in the pre‐departure period than in a control context (i.e., during foraging). Initiators of collective movements grunted more often than followers in the pre‐departure period as well as at individual departure. The latter difference was due to the initiators’ grunt rates increasing earlier than the followers’ and remaining at an elevated level for longer. These observations suggest that grunts serve to coordinate the departure by indicating the individual's readiness to move. The pre‐departure period, in which both initiators and followers showed an elevated grunt rate, may provide the basis for a shared decision on departure time. The difference in initiator and follower call rates suggests that grunts may have a recruitment function, but playback experiments are required to test this potential function. Overall, our study describes how multicontextual close calls can function as movement calls, with changes in call rate providing a potential feedback mechanism for the timing of group movements. This study thus contributes to a more detailed understanding of the mechanisms of group coordination and collective decision‐making.     

Acoustic cues to caller identity in lemurs: a case study

This study investigated the acoustic structure of grunt vocalizations in red-bellied lemurs (Eulemur rubriventer) and its potential for individual discrimination. Acoustic analyses were performed on 1,605 grunts recorded from seven lemurs belonging to two captive groups. From the perspective of sound-filter theory, we described the acoustic structure of grunts, measuring two sets of parameters: fundamental frequency characteristics as larynx-related variables and four formant frequencies as filter-related features. Formants were effective in assigning 80.5% of the vocalizations to the correct emitter against 24.9% scored by the model based on larynx-related variables. We concluded that vocal tract resonances might potentially provide conspecifics with individual cues.     

Expression of Emotional Arousal in Two Different Piglet Call Types

Humans as well as many animal species reveal their emotional state in their voice. Vocal features show strikingly similar correlation patterns with emotional states across mammalian species, suggesting that the vocal expression of emotion follows highly conserved signalling rules. To fully understand the principles of emotional signalling in mammals it is, however, necessary to also account for any inconsistencies in the way that they are acoustically encoded. Here we investigate whether the expression of emotions differs between call types produced by the same species. We compare the acoustic structure of two common piglet calls—the scream (a distress call) and the grunt (a contact call)—across three levels of arousal in a negative situation. We find that while the central frequency of calls increases with arousal in both call types, the amplitude and tonal quality (harmonic-to-noise ratio) show contrasting patterns: as arousal increased, the intensity also increased in screams, but not in grunts, while the harmonicity increased in screams but decreased in grunts. Our results suggest that the expression of arousal depends on the function and acoustic specificity of the call type. The fact that more vocal features varied with arousal in scream calls than in grunts is consistent with the idea that distress calls have evolved to convey information about emotional arousal.     

Experimental Evidence for Phonemic Contrasts in a Nonhuman Vocal System

The ability to generate new meaning by rearranging combinations of meaningless sounds is a fundamental component of language. Although animal vocalizations often comprise combinations of meaningless acoustic elements, evidence that rearranging such combinations generates functionally distinct meaning is lacking. Here, we provide evidence for this basic ability in calls of the chestnut-crowned babbler (Pomatostomus ruficeps), a highly cooperative bird of the Australian arid zone. Using acoustic analyses, natural observations, and a series of controlled playback experiments, we demonstrate that this species uses the same acoustic elements (A and B) in different arrangements (AB or BAB) to create two functionally distinct vocalizations. Specifically, the addition or omission of a contextually meaningless acoustic element at a single position generates a phoneme-like contrast that is sufficient to distinguish the meaning between the two calls. Our results indicate that the capacity to rearrange meaningless sounds in order to create new signals occurs outside of humans. We suggest that phonemic contrasts represent a rudimentary form of phoneme structure and a potential early step towards the generative phonemic system of human language.     

Squirrel monkey chuck call: vocal response to playback chucks based on acoustic structure and affiliative relationship with the caller

Adult female squirrel monkeys (genus Saimiri) that are socially familiar often exchange the chuck vocalization, which differs acoustically across individuals. We used behavioral observations, vocalization playback experiments, and analysis of the acoustic properties of vocalizations to investigate the effect of caller identity and acoustic structure on vocal response to playback chucks in two all-female social groups (n=10 females). Females were most likely to respond with a chuck to the playback chucks of their closely affiliated partners compared to those of nonaffiliated group members. This shows for the first time that the chuck stimulus alone is sufficient to elicit a chuck response from a female's affiliated partner. Additionally, females responded with a chuck mostly to familiar playback chucks from their own group and least to playbacks of silent controls. Unfamiliar playback chucks from the same species and a different squirrel monkey species elicited chuck responses intermediate between familiar chucks and silent controls. Post-hoc discriminant function analyses provide preliminary evidence that females are most likely to respond to unfamiliar chucks when those chucks are close in acoustic structure to familiar chucks from their own social group. These results provide a provisional explanation for error in the squirrel monkey signal processing system, in which unfamiliar chucks never heard before nevertheless elicit a chuck response if they are similar in acoustic structure to familiar group chucks.     

The versatility of graded acoustic measures in classification of predation threats by the tufted titmouse Baeolophus bicolor: exploring a mixed framework for threat communication

Many mammal and bird species respond to predator encounters with alarm vocalizations that generate risk‐appropriate responses in listeners. Two conceptual frameworks are typically applied to the information encoded in alarm calls and to associated anti‐predator behaviors. ‘Functionally referential’ alarm systems encode nominal classes or categories of risk in distinct call types that refer to distinct predation‐risk situations. ‘Risk‐based’ alarms encode graded or ranked threat‐levels by varying the production patterns of the same call types as the urgency of predation threat changes. Recent work suggests that viewing alarm‐response interactions as either referential or risk‐based may oversimplify how animals use information in decision‐making. Specifically, we explore whether graded alarm cues may be useful in classifying risks, supporting a referential decision‐making framework. We presented predator (hawk, owl, cat, snake) and control treatments to captive adult tufted titmice Baeolophus bicolor and recorded their vocalizations, which included ‘chick‐a‐dee’ mobbing calls (composed of chick and D notes), ‘seet’ notes, two types of contact notes (‘chip’, ‘chink’), and song. No single call type was uniquely associated with any treatment and the majority of acoustic measures varied significantly among treatments (46 of 60). The strongest models (ANOVA and classification tree analysis) grouped hawk with cat and owl, and control with snake, and were based on the number or proportion of a) chick and D notes per chick‐a‐dee call, b) chip versus chink notes produced following treatment exposure, and c) the frequency metrics of other note types. We conclude that (1) the predation‐threat information available in complex titmouse alarm calls was largely encoded in graded acoustic measures that were (2) numerous and variable across treatments and (3) could be used singly or in combinations for either ranking or classification of threats. We call attention to the potential use of mixed threat identification strategies, where risk‐based signal information may be used in referential decision‐making contexts.     

Repeated decrease in vocal repertoire size in Streptopelia doves

Most bird species produce different acoustic signals in different behavioural contexts. This intraspecific variation in signal types is thought to be the result of selection for optimal communication in each context. Doves in the genus Streptopelia have three distinct behavioural contexts in which they produce coo vocalizations. Some Streptopelia species have three acoustically similar coo vocalizations associated with the three contexts, but in others the coo vocalizations differ in acoustic structure. Using a well-resolved phylogeny, we examined whether acoustic differentiation between coo types was the ancestral state. Unexpectedly, the results showed that the common ancestor of Streptopelia had differentiated coos rather than a single coo type. This result implies that context-specific acoustic signals disappeared from the vocal repertoire independently at least two times. We further tested whether different context-dependent signal types follow different evolutionary pathways and whether they differ in rate of evolutionary change. We found that the long-range signal (perch-coo) evolves at a higher rate than the short-range signal (bow-coo). These results are discussed in relation to selection for species recognition and transmission requirements.     

Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux's sifakas (Propithecus verreauxi verreauxi)

The production of vocalizations in nonhuman primates is predominantly innate, whereas learning influences the usage and comprehension of vocalizations. In this study, I examined the development of alarm call recognition in free-ranging infant Verreaux's sifakas. Specifically, I investigated their ability to recognize conspecific alarm calls as well as those of sympatric redfronted lemurs (Eulemur fulvus rufus) in Kirindy forest, western Madagascar. Both species have functionally referential alarm calls for aerial predators and give general alarm calls for both aerial and general predators and also other kinds of threats, such as intergroup encounters with conspecifics. I conducted playback experiments with members of two birth cohorts (nine and ten individuals) to determine the age at which infant Verreaux's sifakas discriminate between conspecific alarm calls, heterospecific alarm calls, and non-alarm vocalizations (parrot song). Most 3-4 months old infants fled toward adults after hearing any playback stimuli, whereas 4-5-month-old infants did so only after presentation of alarm calls. Moreover, all infants of these age classes showed a longer latency to flee after the parrot song indicating their emerging ability to discriminate between alarm calls and non-alarm stimuli. At an age of about 6 months, infants switched from fleeing toward adults to performing adult-like escape responses after presentation of conspecific and heterospecific alarm calls. Thus, the ability to discriminate between alarm from non-alarm stimuli precedes the appearance of adult-like responses. The transition to adult-like escape behavior was coincident with the physical independence of infants from their mothers.     

Interactive video playback and opponent assessment in lizards

Video playback has been used to explore many issues in animal communication, but the scope of this work has been constrained by the lack of stimulus-subject interaction. In many natural contexts, each participant's signalling behaviour is dependent from moment-to-moment on that of the other. Analyses of acoustic communication demonstrate the value of reproducing such social contingencies. We assessed the utility of interactive playback for studies of visual signalling by comparing the responses of male Jacky dragons, Amphibolurus muricatus, to interactive and non-interactive digital video playbacks of a life-sized conspecific. Displays produced by lizards in the interactive condition had the effect of suppressing the aggressive display of their simulated opponent. Each stimulus sequence generated during an interactive playback was subsequently played to a size-matched control animal. Males that could interact with the video stimulus responded principally with aggressive displays, while those that could not produced a mixture of aggressive and appeasement signals. Adding a degree of receiver responsiveness is hence sufficient to alter the type of signal evoked, even when video stimuli are physically identical. Interactive playback permits the experimental study of a broader range of theoretical topics and can enhance the realism of video stimuli.