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How vervet monkeys perceive their grunts: Field playback experiments
Anim. Behav., 1982, 30, 739-751
H O W VERVET MONKEYS PERCEIVE THEIR GRUNTS: FIELD PLAYBACK EXPERIMENTS BY D O R O T H Y L. C H E N E Y & ROBERT M. SEYFARTH*
Rockefeller University, Field Research Center, Millbrook, N.Y. 12545 Abstract. 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. Introduction Most studies of animal communication assume that there is a fundamental difference between the use of words by humans and the use of vocalizations by non-human species. The meaning of human words is thought to be highly specific, and, compared with animal signals, relatively independent of context, whereas the meaning of animal signals (insofar as meaning can be determined from the responses signals evoke; Marler 1961) is assumed to be both more general and largely context-dependent (e.g. Marshall 1970; Lancaster 1975; Fry 1977; Smith 1977). Although this view of animal communication is widely accepted, we know surprisingly little about the ways in which the vocalizations of animals, particularly non-human primates, function during social interactions. As a result, there is little direct evidence to support a functional dichotomy between animal signals and human language. Several recent studies, however, suggest that there may be greater complexity than previously imagined in the vocal signals of non-human primates. One of the most common vocalizations of the Japanese macaque (Macacafitscata), for example, is a clear 'coo' call that is used in a variety of social situations. On first examination, all such calls appear to have similar acoustic properties, suggesting that the coos reflect a certain level of arousal, much like a generalized 'contact' call, and that this general call can assume a variety of rneanings depending upon the context in which itis given. Detailed work by Green (1975), *Present address of both authors: Department of Anthropology, University of California, Los Angeles, Calif. 90024
however, has shown that what is initially perceived by the human listener as one uniform acoustical class can in fact be divided into at least seven call types based on consistently different physical properties. Under natural conditions, each call type is correlated with a specific social context, suggesting that the monkeys draw selectively from this class during their social interactions. Thus the animals' repertoire is larger than the human ear initially perceives it to be, and the use of their vocal signals appears to be context-specific (see also Gautier 1974; Lillehei & Snowdon 1978). Similarly, field research on the predator alarm calls of vervet monkeys (Cercopithecus aethiops) suggests that the vocalizations of non-human primates can effectively function to designate objects in the external world. Vervet monkeys give acoustically different alarm calls to each o f their four main predators: leopards, eagles, snakes, and baboons (Struhsaker 1967). Playback experiments using tape-recordings of three of these alarms calls have shown that, even in the absence of actual predators, each alarm type evokes a qualitatively different set of responses from the monkeys (Seyfarth et al. 1980a, b). Because the vervets' alarm calls evoke the same responses as would the predators themselves, the calls may be regarded as a rudimentary form of representational signalling, in which arbitrary, non-iconic signs are used to designate particular referents external to the signaller (Seyfarth et al. 1980a; see also Hockett 1960; Altmann 1967; Savage-Rumbaugh et al. 1980). The prevalence of similar predator-class-specific alarm calls throughout the animal kingdom (e.g. Marler 1956; Ryden 1978; Melchior 1971; 739
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ANIMAL
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Struhsaker 1975) suggests that many animal signals may refer to or 'stand for' events external to the communicator. Alarm calls represent only a small subset of the vervet monkeys' vocal repertoire, and it might be argued that the referential specificity of alarm calls is not representative of the monkeys' entire communication system. Most vocalizations by non-human primates consist of grunts, screams, and chutters, uttered during social interactions with other group members. Do such calls also function to designate events in the external world ? This paper describes a series of playback experiments dealing with the function of vocal signals by vervet monkeys during social interactions. The signal we have chosen for study is a low-pitched, pulsatile grunt, originally described as a 'progression grunt' or 'woof' by Struhsaker (1967, plate 16.3). As Struhsaker noted, this grunt is given in a variety of social contexts. For example, a monkey may grunt as it approaches an individual who is dominant to itself, or as it approaches a subordinate. In some cases, a monkey may grunt as it watches another animal initiate a group movement across an open plain. A grunt may also be given when a monkey has apparently just spotted the members of another group. Even to an experienced human listener, there are no immediately obvious audible differences among grunts, either from one context to another or across individuals (Fig. 1 ; see also Part Two, below). Although the calls may occasionally be answered by a grunt from another monkey, in most cases grunts given in each of the contexts described above evoke no salient behavioural responses. Changes in the direction of gaze, which are difficult to measure under observational conditions, appear to be the only obvious response to grunts. As suggested earlier, the traditional explanation for these grunts would argue that the monkeys use one vocalization in a variety o f contexts. T h e grunt itself is a manifestation of a particular level of arousal, providing information only about the vocalizer's location. Given the rather general nature of the information they convey, any variation in the responses evoked by grunts can be accounted for by variation in the context in which the calls are given. In contrast, Green's (1975) work on Japanese macaques, and our own work on vervet monkey alarm calls (see above), suggest an alternative hypothesis: namely, that what appears to a human listener to be one grunt is in
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fact a number of different grunts. Each grunt type, in and of itself, conveys specific information that is relatively independent of context. In the first .part of this paper, we present results of experiments designed to test between these two hypotlleses. We then present preliminary acoustical analysis of different grunt types, and discuss which acoustical parameters might be used by vervets to distinguish one grunt type from another. Part One Methods
General. In designing experiments to test between the hypotheses outlined above, our general approach was as follows. First, grunts from the same individual were tape-recorded in two or more different and specific contexts (see below). Second, over a period of several months, each of these grunts was played back to a number of different subjects in a variety of social circumstances. Trials were conducted, for example, when there were dominant or subordinate animals nearby, when the group was foraging or resting, and so on. We reasoned that, if the grunts were really one vocalization whose meaning was largely determined by context, subjects should show no consistent differences in responses to the calls. Instead, responses to playback should be a function of the variable contexts in which they were presented. On the other hand, if each of the grunts was different, and if each carried a specific meaning, we should expect consistent differences in responses to each grunt type, regardless of the varying circumstances in which they were played. Our overall method thus involved a series of paired playback experiments in which subjects were asked 'Is grunt A different from grunt B ? If so, is grunt A different from grunt C ? Do grunts B and C differ?', and so on. Study area and subjects. Playback experiments were conducted on three groups of vervet monkeys in Amboseli National Park, Kenya, between January and July, 1980. A description of the park can be found in Altmann & Altmann (1970) and Western & Van Praet (1973). The three study groups occupied adjacent home ranges, and had the following age/sex compositions: group A: five adult males, two adult females, six juveniles (animals aged between one and five years), and two infants (animals under one year of age); group B: one adult male, seven adult females, five juveniles, and one infant; group C: four adult males, four adult females, 11 juveniles, and two infants. All groups
C H E N E Y & S E Y F A R T H . VERVET M O N K E Y VOCALIZATIONS
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had been observed continuously since at least 1977 (Cheney et al. 1981), and all group members could be recognized individually. In this study, dominance ranks of individuals were assigned using methods described in Seyfarth (1980) and Cheney et al. (1981). Observation and recording. On a typical day, two observers spent approximately 2.5 h with each group. Observation sessions were scheduled with the aim of providing a similar amount of data each month on each individual i n each group throughout the day. This requirement dictated the timing of sessions with each group. During each session, both observers sampled behaviour using focal animal and sequence sampling (Altmann 1974). All individuals were sampled for a minimum of 150 rain each month for a total of over 1100 contact hours with all three groups. While sampling animals, each observer tape-recorded as many vocalizations as possible, noting the individuals involved as well as the behaviour immediately preceding and following each utterance. Whenever possible, these data were supplemented with ad libitum recordings. Recordings were m a d e only from known individuals, and were limited to those occasions when the b e h a v i o u r immediately preceding and following the vocalization had been observed. Recordings were made at a distance of 0.5 to 3 m, using either a Nagra III or a Nagra SNN tape recorder at 9.5 cm/s, and Sennheiser directional microphones ( M K H 804 and 805). Grunts chosen as stimuli for playback experi: ments had to satisfy a number of requirements. First, the grunt must originally have been recorded in a relatively unambiguous social context, in which the observer had noted all interactions that preceded and followed the call. Second, because our aim was to test whether or not acoustical differences among grunts were by themselves sufficient to evoke different responses, we attempted to control for variation in call length and amplitude. Only single units of grunts were used as experimental stimuli, and only the grunts of adult females and juveniles were chosen for playback trials: Underl natural conditions, the majority of grunts uttered by members of these age/sex classes occurred in single units (Fig. 1 ; see also Part Two). Thus by limiting our exemplars to single unit calls, our experiments allowed us to determine whether acoustical differences alone affected th'e:: 'mean= ing' of each call. Grunts chosen as Stimuli were similar to one another in duration and ampli-
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tude, both across individuals and across the contexts in which they were originally recorded. Grunts used as stimuli had a mean duration of 0.74 s (SD = 0.14). At the mean distance at which trials were conducted (3.3 m), grunts' had a median sound pressure level of 52 dB (range: 48-56; General Radio ..sound level meter model 1565-B, A weighting)~ Grunts given in response to another grunt were excluded f r o m playback trials. Grunts given as the vocalizer threatened or was threatened by another, or as the vocalizer supplanted or was supplanted by another, were also eliminated. Finally, grunts used as experimental stimuli had to be clearly recorded and free of any additional background vocalizations. Five grunt types were chosen as experimental stimuli, and played to subjects in paired trials. These grunt types were recorded in the five social contexts in which adult females and juveniles most frequently vocalized. For each paired trial, grunts were recorded from the same individual. Grunts were of the following types: (a) Grunt to a dominant male, given by adult females or juveniles of either sex in the vicinity of an adult male who was dominant to them. (b) Grunt to a dominant f e m a l e , given by adult females and juveniles of either sex in the vicinity of an adult female who was dominant to them. (c) Grunt to a subordinate female, given by adult females in the vicinity of an adult female who was subordinate to them. The grunt occurred in the absence of aggressive behaviour on the part of the dominant female. (d) Grunt to a m o n k e y moving into an open area ( M I O ) , givenby adult females and juveniles of either sex as they observed another monkey initiate a group progression onto an open plain. In Amboseli, the vervets' ranges were comprised of bushes and trees, often widely separated by open plains o f short, seasonal grass. Vervets seemed particularly vulnerable to predators when crossing such plains and entering new areas of their range. GrouP progressions into such areas were generally preceded by a period of vigilance, and: animals typically grunted at the first individuals to, initiate, such progressions. (e) Grunt to another ~group, given as adults or juveniles observed members of another group. The grunt usually occurred when the other group had apparently just been spotted. Experimental playbacks., The protocol for playback experiments is summarized in Table I. For each playback series, six individuals in a
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS given group were designated as subjects. Over a period o f several months, these subjects were played each pair o f grunts once. Different individuals acted as subjects only once for a given series o f trials. N o two trials involving subjects in the same group were ever conducted within 24 h o f each other, and trials involving the same subject were separated by a m i n i m u m o f three days. The calls of a given individual were played only to members o f its own group. To the best o f our ability, no experiment was ever conducted when the subject could see the individual whose call was being played. W h e n conducting an experiment, we first decided which grunt was to be played, and which individual would serve as the subject. Anticipating the m o v e m e n t o f the subject, we then selected a likely location and hid a speaker (Nagra D N ) in a bush or tall grass. I f tile subject came to within 3 m o f the speaker, and if all other conditions were satisfied (see above), the trial
began. The mean subject-speaker distance across trials was 3.3 m (SD = 1.3). I n each trial, speaker placement and orientation (that is, the direction in which the grunt was broadcast) were arranged in such a way that we could distinguish between a response in which a subject looked toward the speaker and one in which it oriented its gaze in the direction in which the speaker was pointed. The order in which subjects heard each grunt type was systematically varied, so that no grunt type consistently appeared as the first or second stimulus in any series o f paired trials, T h r o u g h o u t all trials, we attempted to ensure that the experimental protocol mimicked natural conditions as m u c h as possible. Vervets frequently foraged in dense bush near waterholcs or in shrubs and vines at the base o f tree, and they often grunted to one another when they were apparently out o f sight of each other. We therefore felt justified in assuming that a grunt played from a speaker, as if uttered by a monkey behind a bush or trees, was not anomalous.
Table I. Experimental Design
Stimuli tested Series 1 Grunt to subordinate Grunt to dominant
Series 2 Grunt to dominant male Grunt to dominant female
Series3 Grunt to dominant MIO grunt (see text)
Series 4 Grunt to dominant Grunt to another group
Series 5 MIO grunt (see text) Grunt to another group
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Vocalizers
Subjects
Adult female DN (group A)
6 group A animals, all subordinate to DN
Adult female TD (group C)
6 group C animals, all subordinate to TD
Juvenile female LS (group A)
3 group A males (see text)
Adult female TD (group C)
3 group C males (see text)
Juvenile male DS (group A) Adult female DU (group B) Adult female TD (group C)
6 group B animals
6 group A animals
6 group C animals
Adult female DU (group B) Adult female TD (group C) Juvenile female C Y (group C)
6 group B animals 6 group C animals
Adult female DU (group B)
6 group B animals
Adult female TD (group C)
6 group C animals
6 group C animals
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ANIMAL
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Eighty-six per cent of all trials involved a single subject. Exceptions occurred when a second of our predesignated subjects entered the playback area just as a trial began, and unavoidably heard the playback stimulus. In each trial, the subject was filmed with a sound movie camera (Elmo 350SL), for 10 s before and 10 s after the grunt was played. This procedure allowed us to record the grunt on the film sound track, to establish a baseline probability that the subject would show a given behaviour in the absence of a call, and to compare baseline data with the subject's behaviour after playback. A playback experiment was possible on only 10 to 2 0 ~ of all occasions when we prepared to conduct a trial. Attempts to conduct a trial were frustrated when, for example, the predesignated subject moved in an unanticipated direction, away from our chosen location, or when the subject concealed itself in a dense bush. Alternatively, the subject situated itself satisfactorily, but the individual whose grunt was about to be played emerged in full view. In all such cases, the trial was terminated before the grunt was broadcast. Data presented below are drawn from those instances in which a grunt was played and a complete film record obtained. In all playback trials, the movie camera was positioned at either 0, 90, 180, or 270* with respect to both the speaker and the subject. The monkeys' habituation to observers carrying equipment permitted rapid adjustment of the camera's position, and allowed us to control the angle at which trials were filmed. This procedure not only simplified film analysis, but also ensured that we could determine whether or not playbacks caused subjects to orient toward or away from the speaker. The data from each trial consisted of the film record, a narrative commentary spoken into a tape recorder during each trial, and a map drawn to include the position, identity and orientation of the subject, all nearby monkeys, vegetation, the speaker, the movie camera, and the observers. The map also included data on the location, orientation, and behaviour of the individual whose grunt was being played. In scoring the filmed responses to playback, we searched for either qualitative or quantitative differences in the monkeys' responses to different grunts. Responses were defined as follows: Move toward/away from the speaker. These responses were usually unambiguous on film. The minimum criterion for a move was two successive steps by the subject in the same direc-
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tion. If, however, the subject moved parallel to the speaker, so that it approached the speaker before moving away from it, we did not score the subject's response as a move away from the speaker. Scanning. This behaviour fell into four categories: (a) look toward the speaker; (b) look in the direction the speaker was pointed; (c) look in any other direction; (d) look at other monkeys. Animals were scored as having looked in the direction the speaker was pointed when a head movement oriented their gaze along a line parallel to the orientation o f the speaker (for definition of 'looks' see Cheney & Seyfarth 1980; Seyfarth et al. 1980a). A monkey could look at other monkeys at the same time that it looked in a given direction. When a monkey looked at others, their identities were recorded. Two measures were used in scoring films. Latency to respond to a grunt was measured by counting the number of frames from the onset of a grunt on the film sound track to the first indication that a subject began to show a given response. Duration was calculated (see below) using the number of frames, up to a maximum of 180 (10 s), during which a subject showed a given behaviour. Bout lengths were not distinguished in calculating duration (see Seyfarth et al. 1980a, page 1082). To correct for the subject's behaviour before playback, we defined duration of response as the duration of a given behaviour in the 10 s after playback minus the duration of the same behaviour in the 10 s before. Thus i f a subject looked toward the speaker for 36 frames (2 s) b e f o r e playback and for 108 frames (6 s) after playback, the duration of response was scored as 72 frames (4 s). In cases when playback produced no change in behaviour, duration of response was zero. When a subject showed more of a given behaviour before playback than after it, duration of response was scored as negative. Results Grunt to a subordinate versus grunt to a dominant. Six subjects in group A and six subjects
in group C were played grunts that had originally been recorded either as the vocalizer approached a subordinate female or as the vocalizer approached a dominant male (for data on subjects and vocalizers, see Table I). All 12 individuals in both groups were subordinate to the animal whose grunt was being played. In each group, three subjects heard the grunt to a subordinate first, and three subjects heard the
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS grunt to a dominant first. Overall, trials were conducted in a variety of social and environmental circumstances. Playback of grunts produced two kinds of responses: subjects either moved away from the speaker or looked toward the speaker for a longer period following playback than before. Significantly more subjects moved away from the speaker when hearing the grunt to a subordinate than when hearing the grunt to a dominant (Table II). For nine of 12 subjects, the duration of moving away and/or looking toward the speaker was greater following the grunt to a subordinate as opposed to the grunt to a dominant (N = 12, one tie, two-tailed binomial test, P = 0.066). There was no indication that subjects of different ranks responded differently to playbacks of each grunt type. Overall, the grunt to a subordinate evoked both a stronger and a qualitatively different response than the grunt to a dominant, suggesting that the two calls conveyed consistently different information. As mentioned above (see Methods), we attempted to conduct all trials at a time when, to the best of our knowledge, subjects were out of sight of the individual whose call was being played. Nevertheless, it might be argued that differences in the response to each grunt type occurred not because each grunt conveyed different information, but because the location of the original vocalizer was consistently different for each grunt type. With this in mind, we examined our records, but found no evidence that playbacks increased the probability that subjects would look toward the individual whose call was being played. Grunt to a dominant male versus grunt to a dominant female. The difference in the responses
of subjects to grunts given to a subordinate and grunts given to a dominant may have resulted in part because, regardless of the relative ranks of the animals involved, one grunt was originally given to a female while the other was originally Table H. Responses to Playback of Grunt to Subordinate and Grunt to Dominant
Move away from speaker after playback Yes
No
Grunt to subordinate
5
7
Grunt to dominant
0
12
Fisher Exact Probability Test (two-tailed), P < 0.05.
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given to a male. In order to determine whether vocalizers gave different grunts to dominant animals depending upon those animals' sex, we designed a second series of experiments. In this series, six adult males (three from group A, three from group C) were played grunts that had originally been given by a female member of their group either as she approached a dominant male or as she approached a dominant female (Table I). All six subjects were subordinate to the male but dominant to the female. We reasoned that, if a vocalizer gave different grunts to dominant animals depending on their sex, subjects should respond more strongly to the grunt given to the male than to the grunt given to the female. Playback of the two grunt types produced one consistent response: subjects looked toward the speaker for a longer time following playback than before. There was no significant difference, however, between the two grunts in the duration that subjects looked toward the speaker (MannWhitney U-test, N1 = 6, N~ = 6, U = 17.5, P > 0.10). Results suggested that, when giving grunts to dominant animals, vervets did not distinguish between males and females. Grunt to a dominant versus grunt to an animal moving into an open area ( M I O ) . In our third
series of trials, six subjects in each of the three study groups were played grunts that had originally been given by a member o f their group either as it approached a dominant or as it watched another monkey move into an open area (MIO). As before, the order of stimulus presentation, as well as the location of the speaker relative to subjects, were varied throughout all trials (Table I). Results gave no indication that playbacks caused subjects to look at the individual whose call was being played. There were consistent differences, however, in the responses evoked by the two grunts. When compared with the MIO grunt, playback of grunts to a dominant produced significantly longer durations of looking toward the speaker (Fig. 2). The subjects again behaved as if the two grunts conveyed consistently different information. Grunt to a dominant versus grunt to another group. Six subjects in group B and 12 subjects
in group C were played grunts that had originally been given by a member of their group either as it approached a dominant or as it looked at another group (Table I). In these trials, grunts to another group produced significantly longer durations of looking in the direction the
ANIMAL
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BEHAVIOUR,
speaker was pointed than did grunts to a dominant (Fig. 3). It should be emphasized ~hat the response of looking in the direction the speaker was pointed did not occur because subjects looked toward the animal whose call was being played. More-
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Fig. 2. D u r a t i o n o f responses to playback of g r u n t to d o m i n a n t a n d M I O grunt. Y-axis s h o w s d u r a t i o n o f res p o n s e (defined in text), m e a s u r e d in frames of films at 18 fps. H i s t o g r a m s show m e a n s plus s t a n d a r d errors for subjects. Probability value based o n two-tailed M a n n W h i t n e y UXtest. L o o k toward speaker: N~ = 18, N2 = 18, U = 100, P < 0.05. L o o k in direction speaker is pointed: U = 137, P > 0.10.
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over, the response was not simply due to an increase in scanning behaviour, since neither grunt significantly increased the duration of looking in directions other than the one in which the speaker was pointed. This is not to say that our data indicated the precise point toward which animals were looking. The film analysis permitted us to specify only four directions of orientation (see Methods). In summary, therefore, grunts to another group seemed to serve a rather specific 'alerting' function, directing the listener's attention away from the vocalizer and toward the area in which the vocalizer would ordinarily have been facing. M I O grunt versus grunt to another group. Finally, we compared the responses of six subjects in group B and six subjects in group C to the MIO grunt and the grunt to another group (Table I). In previous trials, these two grunts had elicited similar responses. Both produced a a slight increase in the duration of looking toward the speaker, as well as a slight increase in the duration of looking in the direction the speaker was pointed (Figs 2, 3). Thus it was not surprising to find no difference in the duration of responses elicited when the two calls were compared directly (Fig. 4). Nevertheless, other evidence suggested that the grunts evoked measurably different responses. Grunts to another group showed a shorter latency to elicit looking in the direction the speaker was pointed, while MIO grunts showed
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Fig. 3. D u r a t i o n o f responses to playback o f g r u n t to d o m i n a n t a n d g r u n t to a n o t h e r group. Legend as in Fig. 2. L o o k toward speaker: N t = 18, N~ = 17, U = 111.5, P > 0.10. L o o k in direction speaker is pointed: U -- 91, P < 0.05.
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Fig. 4. D u r a t i o n o f responses to p l a y b a c k o f M I O a n d g r u n t to a n o t h e r group. L e g e n d as in Fig. 2. toward speaker: N1 = 12, N2 = 11, U = 47.5, P > L o o k in direction speaker is pointed: U = 42, P >
grunt Look 0.10. 0.10.
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS a shorter latency to elicit looking ~ the speaker (Fig. 5). While each of these differences only approached significance (P < 0.07), they represented changes in two opposing behaviourai measures. Moreover, no other comparisons of different grunt types revealed any differences in the latency to elicit a given response. While not statistically significant, the M I O grunt and the grunt to another, group appeared to differ in their ability to produce a particular response, suggesting that the two calls may have conveyed different information to the monkeys. Part Two In experiments described in Part One, the responses'of subjects suggested that vervet monkeys distinguished among at least four different grunt types. Even to an experienced human listener, however, there were no immediately salient acoustical distinctions among the various grunt types. Subsequent laboratory analysis was therefore conducted to determine what acoustical cues might have been used by vervets to distinguish among different grunts. Methods
In order to conduct an accurate statistical analysis of the acoustical variants within and Grunt To: MIO P<.07
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Fig. 5. Latency of subjects to respond to MIO grunt and grunt to another group. Y-axis shows latency to respond, measured in number of fraraes of film at 18 fps. Otherwise legend as in Fig. 2. Look toward speaker: N1 = 12, N2 = 9, U = 27, P < 0.07. Look in direction speaker is pointed: N1 = 12, N2 = I0, U -~ 31, P < 0.07. Animals who were looking toward the speaker or in the direction the speaker was pointed at the onset of playback have been exclud from analysis.
747
between the four grunt types described earlier, we required high quality exemplars from a number o f individuals, each of whom had been taperecorded a number of times in each of the four different contexts. Only under these conditions was: it possible to compare the acoustical properties of grunts given in different social contexts while simultaneously controlling for individual variation (Lillehei & Snowdon 1978). Examination of field recordings made in 1977, 1978, and 1980 revealed six individuals (all adult females) for whom these requirements were met. For each of these individuals, we had between five and 10 recordings of grunts given in each of the four contexts described above. Analysis of the acoustical properties of grunts was conducted with tape at normal and 1/4 speed, using a Kay sonagraph model 7029A, with a wide (300 Hz) or narrow (45 Hz) band filter, the FL1 shaping selector, and a frequency scale of 80-8000 Hz. More detailed spectral information was obtained using the computer system described by Zoloth et al. (1980), where the 256-point fast F o u r i e r transform has a minimum frequency resolution of 76.9 Hz. Power spectra taken over the entire duration of the call allowed accurate assessment of overall frequency peaks, while spectra taken of the first, second, and final third of each call allowed t~s to measure frequency modulation. Analysis was conducted on calls that had been corrected for the 'presence of background noise. This correction was made by first taking a power spectrum of the call, including its background noise, then taking a power spectrum of the background noise alone in the 100 ms preceding the call, and finally subtracting the latter from the former using the noise correction formula described by Peterson & Gross (t978). In the following section, the terms unit and call are defined as in Struhsaker (!967). As a first step in the acoustical analysis of grunt types, we examined the grunts given by one female (TD of group C) in the four contexts described above: when approaching a dominant, when approaching a subordinate, when watching another animal move into an open area (MIO), and when looking at another group. Sixteen acoustical features were measured. For each measure, an overall statistical test (either Chi-square or one-way analysis of variance) was used to determine the degree o f heterogeneity across call types. I f an acoustical feature showed significant heterogeneity across grunt types, we concluded that monkeys might potentially make
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ANIMAL
BEHAVIOUR,
use o f the feature when distinguishing a m o n g grunts. As a second step in o u r analysis, we r e p e a t e d these tests using grunts f r o m five o t h e r a d u l t females: A P (group C), M P , D N , a n d LB (group A ) ; a n d D U (group B). Vocalizations f r o m each i n d i v i d u a l were analysed separately, following the p r o c e d u r e originally d e v e l o p e d for T D ' s grunts. Results
A s described above, we b e g a n by a n a l y s i n g the grunts o f one a d u l t female, T D . T h e m e a -
30,
3
sures tested, statistical tests used, a n d results are shown in T a b l e I I I (left-hand column). T a b l e I I I also s u m m a r i z e s the results o f similar analyses p e r f o r m e d on the five other females (righth a n d column). These results a r e described in greater detail below. T D ' s grunts, as well as those o f o t h e r vervet m o n k e y s , a p p e a r e d on a frequency versus time d i s p l a y as r a t h e r noisy, n o n - t o n a l sounds (Fig. 1 ; see also S t r u h s a k e r 1967, plate 16). N e v e r t h e less, detailed analysis revealed a n u m b e r o f acoustical measures t h a t c o u l d p o t e n t i a l l y a l l o w a listener to distinguish a m o n g grunts given in
Table HI. The Acoustical Features that Differentiated among Grunts Given by Adult Female TD (Left Columns) and Five Other Adult Females (Right Column) in Four Different Contexts
Adult female TD Acoustical feature tested
Test used
Result
Also significant for:
1. 2.
Call length Peak frequency
Anova Anova
P < 0.01 P < 0.01
LB AP, MP, DN, LB
3.
Amplitude difference between peaks
Anova
P < 0.01
AP, MP, DN, LB
4.
Presence/absence of 3rd frequency peak within 5 dB of strongest peak
X2
P < 0.01
5.
Frequency modulation of amplitude peak ~< 500 Hz
X~
NS
6.
Frequency modulation of amplitude peak between 500 and 1500 Hz
Z~
P < 0.05
7.
Number of units/call
Anova
P < 0.01
8.
Number of calls with amplitude peak in 1st unit
X2
NS
9.
Number of units with amplitude peak in 1st half
X2
NS
10.
Number of calls where unit with peak amplitude has amplitude peak in 1st half
X~
NS
11.
Unit length
Anova
P < 0.01
12.
Inter-unit interval
Anova
NS
13.
Pulse rate
Anova
NS
14.
Frequency of amplitude peak between 500 and 1500 Hz
Anova
NS
15.
Frequency separation between adjacent peaks
Anova
NS
16.
Changes in pulse rate within units over time
X~
P < 0.01
All probability values are two-tailed. NS
=
P > 0.10.
AP, MP, DN, DU
AP, DU, LB AP
AP, DN, LB
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS different contexts. TD's grunt to a dominant, for example, contained o n e frequency peak, usually around 310 Hz. Grunts to a subordinate, MIO grunts, and grunts to another group contained a second peak, usually between 690 and 1500 Hz. In grunts to a subordinate the two peaks were of roughly equal amplitude. In M I O grunts the lower peak was stronger, while in grunts to another group the upper peak was stronger (Fig. 6; measures 2 and 3 in Table III). Each of these measures showed significant heterogeneity across grunt types (Table III), suggesting that these acoustical parameters could have been used to distinguish among TD's grunts. Additional analysis revealed a number of other parameters that distinguished TD's different grunt types. The MIO grunt was significantly more likely than all others to have an upper frequency peak that rose from the first to the second and fi'om the second to the final third of each call (measure 6, Table III). In grunts to a dominant and grunts to a subordinate, pulse rate generally decreased within each unit (see Fig. 1), while pulse rate increased or remained constant in M I O grunts and grunts to another group (measure 16, Table III). In order to determine whether the acoustical parameters t h a t permitted us to distinguish among TD's grunts remained constant across individuals, a second sample of recordings from five other adult females was analysed as outlined above. Of the 16 measures tested, seven
-Io
-20
In, 0
io
(b)
- o
1.0
2.0
:-. 0
1.0
749
were non,significant across grunt types for all five females, and three others were significant for only one female (Table III), Two measures showed significant differences for four females, and three were significant for five females. For at least some acoustical measures, therefore, there were consistent differences among individual grunt types, both across individuals and across groups. Precisely which of these acoustical distinctions were actually used by the monkeys remains to be determined. A more detailed analysis o f the different grunt types is currently in progress. The preliminary results described here, however, indicate two points of interest. First, some acoustical features were more likely than others to show heterogeneity across g r u n t types. Second, there was considerable 'agreement" among adult females in the acoustical cues that distinguished among different grunts. Discussion
The results of the field playback experiments are summarized in Table IV. In examining this table, it should be remembered that grunts to a subordinate were the only grunts tested that elicited movement away from the speaker (Table II). Thus although grunts to a subordinate were only compared directly against grunts to a dominant, there was indirect evidence that the monkeys would also distinguish grunts to a subordinate from M I O grunts and grunts to another group. Similarly, responses elicited by grunts to a dominant, MIO grunts, and grunts to another group could all be distinguished from one another by at least one behavioural Table IV. A Summary of Significant Differences between the Responses Evoked by Different Grunts
2.0
Grunt to:
Frequency (kHz)
Another
E
Subordinate Dominant MIO Subordinate Dominant -20
, 0
1.0
- 20
9 ~ 2.0
[
j:
0
I.(3
MIO
1
group
(Not tested) 2
4 (3), (5)
210
Frequency (kHz)
Fig. 6. Power spectra of four grunts given by the same individual (adult female TD) (a) when approaching a dominant, (b) when approaching a subordinate, (c) when watching another animal move into an open area (MIO), and (d) when looking at another group. Power spectra have been corrected for background noise (see text).
Measures tested were: (1) move away from the speaker; (2) duration of looking toward the speaker; (3) latency to look toward the speaker; (4) duration of looking in the direction speaker pointed; (5) latency to look in the direction speaker pointed. Entries in each cell indicate a significant difference at the 0.05 level. Entries in parerstheses indicate a level of significance of 0.07. All tests are two-tailed.
750
ANIMAL
BEHAVIOUR,
measure. Results suggest that each grunt type, like each of the vervets' alarm calls (Seyfarth et al. 1980a), transmits different and specific information. In this respect, the grunts appear to function in a rudimentary representational manner. Despite such outward similarities, however, the vervets' grunts are in many respects more subtle than their alarm calls. Alarm calls, for example, are easily distinguished by the human ear, whereas even a practised listener finds it difficult to tell one grunt type from another. Preliminary acoustical analysis has revealed a number of measures by which grunt types can potentially be distingushed from each other, but these measures are by no means as obvious as the acoustical distinctions among alarm calls. In an analogous manner, the alarm calls that vervets give to different predators evoke easily observable, qualitatively different responses from other monkeys (Seyfarth et al. 1980a), while the different responses evoked by different grunt types are much less easily distinguished. Distinctions among responses to different grunt types in playback trials were generally quantitative rather than qualitative: subjects showed more of a given response, or responded more quickly, when hearing one grunt type as opposed to another. Although only five grunt types were used as experimental stimuli, there is no reason to believe that the diversity of vervet grunts is restricted to the exemplars discussed here. Results of playback experiments support the hypothesis that the vocal repertoire of non-human primates, when assessed by the primates themselves, may be f a r larger than classification by human ear would suggest (see also Green 1975; Zoloth et al. 1979). There is s o m e evidence, then, that vervet monkey grunts transmit specific information, and that in some cases they may act as if they refer to external objects or events, such as another group, or a monkey moving into an open area. Do vervet grunts therefore resemble human words, so that when a monkey grunts it has a mental representation of some object or concept that it wishes to communicate (see e.g. SavageRumbaugh et al. 1980) ? Clearly, our data cannot address this question, since the experiments measured only the responses evoked by each grunt type. Such responses revealed nothing about the vocalizer's internal representation of interactions or objects. Nevertheless, the consistent differences in responses to each grunt type
30,
3
suggest that each grunt transmitted different infbrmation to the monkeys, without requiring full support of contextual cues (see also Premack 1973, 1975). This is not to say that contextual variables (including the vocalizer's own behaviour) are irrelevant in determining the 'meaning' of a grunt to other monkeys. Contextual components are doubtless important for the interpretation of grunts by vervets, just as contextual cues enrich the meaning of words for humans. Experiments suggest, however, that in many cases monkeys make less use of contextual cues than they do of acoustical features when interpreting the 'meaning' of a call. Although the playback experiments described here suggest that vervet monkeys may be capable of rudimentary representational signalling, they do not explain why natural selection might have favoured the use of such signals during social interactions. While it is not difficult to imagine the advantage of developing different alarm calls for predators with different modes of hunting, the benefits of such representational signalling within the group are less clear. The social environment within groups of Old World monkeys demands that individuals be able to make complex classifications of the bonds and relationships of other group members, and act adaptively on the basis of their extrapolations (Humphrey 1976; Seyfarth & Cheney, in press). It seems possible that the evolution of complex signal forms may have been favoured by the selective pressures placed on individuals by their fellow group members. The use of different calls in different contexts involves not only a reduction of uncertainty and ambiguity, but also an increase in the amount of information that can be conveyed to (or withheld from) others. Only by studying vocalizations within the broader context of other forms of social interactions, and by considering what primates need to signal about, will it be possible to begin to understand the selective forces that might have favoured the evolution of representational signalling.
Acknowledgments We thank the Office of the President and the Ministry of Tourism and Wildlife of the Republic of Kenya for permission to work in Amboseli National Park. We are especially grateful to B. Oguya, the Warden of Amboseli during this research project, for his kind assistance and cooperation. S. Green, S. Gilmore, H. and S.
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS Gouzoules, P. Marler, M. Petersen, a n d T. Struhsaker read earler drafts of this manuscript, a n d we t h a n k them for their c o m m e n t s a n d criticism. I n presenting these results at seminars, we also benefited from the c o m m e n t s of R. Dooling, F. N o t t e b o h m , a n d H. Terrace. Finally, we t h a n k P. Marler a n d F. N o t t e b o h m for their l o a n o f field equipment. Research was supported by the H. F. G u g g e n h e i m F o u n d a t i o n , N S F g r a n t BNS 80-08946, a n d N S F g r a n t BNS 7716894 to P. Marler. REFERENCES
Altmann, J. 1974. Observational study of behaviour: sampling methods. Behaviour, 49, 227-267. Altmann, S. A. 1967. The structure of primate social communication. In: Social Communication among Primates (Ed. by S. A. Altmann), pp. 352-362. Chicago: University of Chicago Press. Altmann, S. A. & Altmann, J. 1970. Baboon Ecology. Chicago: University of Chicago Press. Cheney, D. L. & Seyfarth, R. M. 1980. Vocal recognition in free-ranging vervet monkeys. Anita. Behav., 28, 362-367. Cheney, D. L., Lee, P. C. & Seyfarth, R. M. 1981; Behavioral correlates of non-random mortality among free-ranging female vervet monkeys. Behav. Ecol. Sociobiol., 9, 153-161. Fry, D. 1977. Homo Loquens: Man as a Talking Animal. Cambridge: Cambridge University Press. Gautier, J. -P. 1974. Field and laboratory studies of talapoin monkeys (Miopithecus talapoin). Behaviour, 51, 209.-273. Green, S. 1975. Communication by a graded vocal system in Japanese monkeys. In: Primate Behavior, VoL 4 (Ed. by L. A. Rosenblum), pp. 1,102. New York: Acadernic Press. Hockett, C. F. 1960. Logical consideration in the study of animal communication. In: Animal Sounds and Communication (Ed. by W. E. Lanyon & W. N. Tavolga), pp. 292-340. Washington, D.C. : A.I.B.S. Humphrey, N. K. 1976. The social function of intellect. In: Growing Points in Ethology (Ed. by P. P. G. Bateson & R. A. Hinde), pp. 303-317. Cambridge: Cambridge University Press. Lancaster, J. 1975. Primate Behavior and the Emergence of Human Culture. New York: Holt, Rinehart & Winston. Lillehei, R. A. & Snowdon, C. T. 1978. Individual and situational differences in the vocalizations of young stumptail macaques (Macaca arctoides). Behaviour, 65, 270-281. Marler, P. 1956. The voice of the chaffinch and its function as a language. Ibis, 98, 231-261. Marler, P. 1961. The logical analysis of animal communication. J. theor. Biol., 1, 295-317.
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Marshall, J. C. 1970. The biology of communication in man and animals. In: New Horizons in Linguistics (Ed. by J. Lyons), pp. 229-241. Harmondsworth: Penguin. Melchior, H. R. 1971. Characteristics of arctic ground squirrel alarm calls. Oecologia, 7, 184-190. Peterson, A. P. & Gross, E. E. 1978. Handbook of Noise Measurement. Concord: General Radio Publ. Co. Premack, D. 1973. Concordant preferences as a precondition for affective but not symbolic communication. Cognition, I, 251-264. Premack, D. 1975. On the origins of language, in: Hamtbook of Psychobiology (Ed. by M. S. Gazzaniga & C. B. Blakemore), pp. 591-605. New York: Academic Press. Ryden, O. 1978. Differential responsiveness of great tit nestlings~Parus major, to natural auditory stimuli. Z. Tierpsychol., 47, 236-253. Savage-Rumbaugh, E. S., Rumbaugh, D. M., Smith, S. T. & Lawson, J. 1980. Reference: the linguistic essential. Science, N. Y., 210, 922-925. Seyfarth, R. M. 1980. The distribution of grooming and related behaviours among adult female vervet monkeys. Anita. Behav., 28, 798-813. Seyfarth, R. M. & Cheney, D. L. In press. How monkeys see the world: a review of recent research on East African vervet monkeys. In: Primate Communication (Ed. by C. Snowdon, C. Brown & M. Petersen). Cambridge: Cambridge University Press. Seyfarth, R. M., Cheney, D. L. & Marler, P. 1980a. Vervet monkey alarm calls: semantic communication in a free-ranging primate. Anita. Behav., 28, 1070-1094. Seythrth, R. M., Cheney, D. L. & Marler, P. 1980b. Monkey responses to three different alarm calls: evidence for predator classification and semantic communication. Science, N. Y., 210, 801-803. Smith, W. J. 1977. The Behavior of Communicating. Cambridge, Mass.: Harvard University Press. Struhsaker, T. T. 1967. Auditory communication among vervet monkeys (Cercopithecus aethiops). In: Social Communication among Primates (Ed. by S. A. Altmann), pp. 281-324. Chicago: University of Chicago Press. Struhsaker, T. T. 1975. The Red Colobus Monkey Chicago: University of Chicago Press. Western, D. & Van Praet, C. 1973. Cyclical changes in the habitat and climate of an East African ecosystem. Nature, Loud., 241, 104-106. Zoloth, S. R., Petersen, M. R., Beecher, M. D., Green, S., Marler, P., Moody, D. B. & Stebbins, W. 1979. Species-specific perceptual processing of vocal sounds by monkeys, Science, N. Y., 204, 870-873. Zoloth, S. R., Dooling, R., Miller, R. & Peters, S. 1980. A minicomputer system for the synthesis of animal vocalizations. Z. Tierpsychol., 54, 151-162. (Received 3 July 1981 ; revised 11 December 1981 ; MS. number: A2683)
H O W VERVET MONKEYS PERCEIVE THEIR GRUNTS: FIELD PLAYBACK EXPERIMENTS BY D O R O T H Y L. C H E N E Y & ROBERT M. SEYFARTH*
Rockefeller University, Field Research Center, Millbrook, N.Y. 12545 Abstract. 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. Introduction Most studies of animal communication assume that there is a fundamental difference between the use of words by humans and the use of vocalizations by non-human species. The meaning of human words is thought to be highly specific, and, compared with animal signals, relatively independent of context, whereas the meaning of animal signals (insofar as meaning can be determined from the responses signals evoke; Marler 1961) is assumed to be both more general and largely context-dependent (e.g. Marshall 1970; Lancaster 1975; Fry 1977; Smith 1977). Although this view of animal communication is widely accepted, we know surprisingly little about the ways in which the vocalizations of animals, particularly non-human primates, function during social interactions. As a result, there is little direct evidence to support a functional dichotomy between animal signals and human language. Several recent studies, however, suggest that there may be greater complexity than previously imagined in the vocal signals of non-human primates. One of the most common vocalizations of the Japanese macaque (Macacafitscata), for example, is a clear 'coo' call that is used in a variety of social situations. On first examination, all such calls appear to have similar acoustic properties, suggesting that the coos reflect a certain level of arousal, much like a generalized 'contact' call, and that this general call can assume a variety of rneanings depending upon the context in which itis given. Detailed work by Green (1975), *Present address of both authors: Department of Anthropology, University of California, Los Angeles, Calif. 90024
however, has shown that what is initially perceived by the human listener as one uniform acoustical class can in fact be divided into at least seven call types based on consistently different physical properties. Under natural conditions, each call type is correlated with a specific social context, suggesting that the monkeys draw selectively from this class during their social interactions. Thus the animals' repertoire is larger than the human ear initially perceives it to be, and the use of their vocal signals appears to be context-specific (see also Gautier 1974; Lillehei & Snowdon 1978). Similarly, field research on the predator alarm calls of vervet monkeys (Cercopithecus aethiops) suggests that the vocalizations of non-human primates can effectively function to designate objects in the external world. Vervet monkeys give acoustically different alarm calls to each o f their four main predators: leopards, eagles, snakes, and baboons (Struhsaker 1967). Playback experiments using tape-recordings of three of these alarms calls have shown that, even in the absence of actual predators, each alarm type evokes a qualitatively different set of responses from the monkeys (Seyfarth et al. 1980a, b). Because the vervets' alarm calls evoke the same responses as would the predators themselves, the calls may be regarded as a rudimentary form of representational signalling, in which arbitrary, non-iconic signs are used to designate particular referents external to the signaller (Seyfarth et al. 1980a; see also Hockett 1960; Altmann 1967; Savage-Rumbaugh et al. 1980). The prevalence of similar predator-class-specific alarm calls throughout the animal kingdom (e.g. Marler 1956; Ryden 1978; Melchior 1971; 739
740
ANIMAL
BEHAVIOUR,
Struhsaker 1975) suggests that many animal signals may refer to or 'stand for' events external to the communicator. Alarm calls represent only a small subset of the vervet monkeys' vocal repertoire, and it might be argued that the referential specificity of alarm calls is not representative of the monkeys' entire communication system. Most vocalizations by non-human primates consist of grunts, screams, and chutters, uttered during social interactions with other group members. Do such calls also function to designate events in the external world ? This paper describes a series of playback experiments dealing with the function of vocal signals by vervet monkeys during social interactions. The signal we have chosen for study is a low-pitched, pulsatile grunt, originally described as a 'progression grunt' or 'woof' by Struhsaker (1967, plate 16.3). As Struhsaker noted, this grunt is given in a variety of social contexts. For example, a monkey may grunt as it approaches an individual who is dominant to itself, or as it approaches a subordinate. In some cases, a monkey may grunt as it watches another animal initiate a group movement across an open plain. A grunt may also be given when a monkey has apparently just spotted the members of another group. Even to an experienced human listener, there are no immediately obvious audible differences among grunts, either from one context to another or across individuals (Fig. 1 ; see also Part Two, below). Although the calls may occasionally be answered by a grunt from another monkey, in most cases grunts given in each of the contexts described above evoke no salient behavioural responses. Changes in the direction of gaze, which are difficult to measure under observational conditions, appear to be the only obvious response to grunts. As suggested earlier, the traditional explanation for these grunts would argue that the monkeys use one vocalization in a variety o f contexts. T h e grunt itself is a manifestation of a particular level of arousal, providing information only about the vocalizer's location. Given the rather general nature of the information they convey, any variation in the responses evoked by grunts can be accounted for by variation in the context in which the calls are given. In contrast, Green's (1975) work on Japanese macaques, and our own work on vervet monkey alarm calls (see above), suggest an alternative hypothesis: namely, that what appears to a human listener to be one grunt is in
30,
3
fact a number of different grunts. Each grunt type, in and of itself, conveys specific information that is relatively independent of context. In the first .part of this paper, we present results of experiments designed to test between these two hypotlleses. We then present preliminary acoustical analysis of different grunt types, and discuss which acoustical parameters might be used by vervets to distinguish one grunt type from another. Part One Methods
General. In designing experiments to test between the hypotheses outlined above, our general approach was as follows. First, grunts from the same individual were tape-recorded in two or more different and specific contexts (see below). Second, over a period of several months, each of these grunts was played back to a number of different subjects in a variety of social circumstances. Trials were conducted, for example, when there were dominant or subordinate animals nearby, when the group was foraging or resting, and so on. We reasoned that, if the grunts were really one vocalization whose meaning was largely determined by context, subjects should show no consistent differences in responses to the calls. Instead, responses to playback should be a function of the variable contexts in which they were presented. On the other hand, if each of the grunts was different, and if each carried a specific meaning, we should expect consistent differences in responses to each grunt type, regardless of the varying circumstances in which they were played. Our overall method thus involved a series of paired playback experiments in which subjects were asked 'Is grunt A different from grunt B ? If so, is grunt A different from grunt C ? Do grunts B and C differ?', and so on. Study area and subjects. Playback experiments were conducted on three groups of vervet monkeys in Amboseli National Park, Kenya, between January and July, 1980. A description of the park can be found in Altmann & Altmann (1970) and Western & Van Praet (1973). The three study groups occupied adjacent home ranges, and had the following age/sex compositions: group A: five adult males, two adult females, six juveniles (animals aged between one and five years), and two infants (animals under one year of age); group B: one adult male, seven adult females, five juveniles, and one infant; group C: four adult males, four adult females, 11 juveniles, and two infants. All groups
C H E N E Y & S E Y F A R T H . VERVET M O N K E Y VOCALIZATIONS
741
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S Z
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742
ANIMAL
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had been observed continuously since at least 1977 (Cheney et al. 1981), and all group members could be recognized individually. In this study, dominance ranks of individuals were assigned using methods described in Seyfarth (1980) and Cheney et al. (1981). Observation and recording. On a typical day, two observers spent approximately 2.5 h with each group. Observation sessions were scheduled with the aim of providing a similar amount of data each month on each individual i n each group throughout the day. This requirement dictated the timing of sessions with each group. During each session, both observers sampled behaviour using focal animal and sequence sampling (Altmann 1974). All individuals were sampled for a minimum of 150 rain each month for a total of over 1100 contact hours with all three groups. While sampling animals, each observer tape-recorded as many vocalizations as possible, noting the individuals involved as well as the behaviour immediately preceding and following each utterance. Whenever possible, these data were supplemented with ad libitum recordings. Recordings were m a d e only from known individuals, and were limited to those occasions when the b e h a v i o u r immediately preceding and following the vocalization had been observed. Recordings were made at a distance of 0.5 to 3 m, using either a Nagra III or a Nagra SNN tape recorder at 9.5 cm/s, and Sennheiser directional microphones ( M K H 804 and 805). Grunts chosen as stimuli for playback experi: ments had to satisfy a number of requirements. First, the grunt must originally have been recorded in a relatively unambiguous social context, in which the observer had noted all interactions that preceded and followed the call. Second, because our aim was to test whether or not acoustical differences among grunts were by themselves sufficient to evoke different responses, we attempted to control for variation in call length and amplitude. Only single units of grunts were used as experimental stimuli, and only the grunts of adult females and juveniles were chosen for playback trials: Underl natural conditions, the majority of grunts uttered by members of these age/sex classes occurred in single units (Fig. 1 ; see also Part Two). Thus by limiting our exemplars to single unit calls, our experiments allowed us to determine whether acoustical differences alone affected th'e:: 'mean= ing' of each call. Grunts chosen as Stimuli were similar to one another in duration and ampli-
30,
3
tude, both across individuals and across the contexts in which they were originally recorded. Grunts used as stimuli had a mean duration of 0.74 s (SD = 0.14). At the mean distance at which trials were conducted (3.3 m), grunts' had a median sound pressure level of 52 dB (range: 48-56; General Radio ..sound level meter model 1565-B, A weighting)~ Grunts given in response to another grunt were excluded f r o m playback trials. Grunts given as the vocalizer threatened or was threatened by another, or as the vocalizer supplanted or was supplanted by another, were also eliminated. Finally, grunts used as experimental stimuli had to be clearly recorded and free of any additional background vocalizations. Five grunt types were chosen as experimental stimuli, and played to subjects in paired trials. These grunt types were recorded in the five social contexts in which adult females and juveniles most frequently vocalized. For each paired trial, grunts were recorded from the same individual. Grunts were of the following types: (a) Grunt to a dominant male, given by adult females or juveniles of either sex in the vicinity of an adult male who was dominant to them. (b) Grunt to a dominant f e m a l e , given by adult females and juveniles of either sex in the vicinity of an adult female who was dominant to them. (c) Grunt to a subordinate female, given by adult females in the vicinity of an adult female who was subordinate to them. The grunt occurred in the absence of aggressive behaviour on the part of the dominant female. (d) Grunt to a m o n k e y moving into an open area ( M I O ) , givenby adult females and juveniles of either sex as they observed another monkey initiate a group progression onto an open plain. In Amboseli, the vervets' ranges were comprised of bushes and trees, often widely separated by open plains o f short, seasonal grass. Vervets seemed particularly vulnerable to predators when crossing such plains and entering new areas of their range. GrouP progressions into such areas were generally preceded by a period of vigilance, and: animals typically grunted at the first individuals to, initiate, such progressions. (e) Grunt to another ~group, given as adults or juveniles observed members of another group. The grunt usually occurred when the other group had apparently just been spotted. Experimental playbacks., The protocol for playback experiments is summarized in Table I. For each playback series, six individuals in a
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS given group were designated as subjects. Over a period o f several months, these subjects were played each pair o f grunts once. Different individuals acted as subjects only once for a given series o f trials. N o two trials involving subjects in the same group were ever conducted within 24 h o f each other, and trials involving the same subject were separated by a m i n i m u m o f three days. The calls of a given individual were played only to members o f its own group. To the best o f our ability, no experiment was ever conducted when the subject could see the individual whose call was being played. W h e n conducting an experiment, we first decided which grunt was to be played, and which individual would serve as the subject. Anticipating the m o v e m e n t o f the subject, we then selected a likely location and hid a speaker (Nagra D N ) in a bush or tall grass. I f tile subject came to within 3 m o f the speaker, and if all other conditions were satisfied (see above), the trial
began. The mean subject-speaker distance across trials was 3.3 m (SD = 1.3). I n each trial, speaker placement and orientation (that is, the direction in which the grunt was broadcast) were arranged in such a way that we could distinguish between a response in which a subject looked toward the speaker and one in which it oriented its gaze in the direction in which the speaker was pointed. The order in which subjects heard each grunt type was systematically varied, so that no grunt type consistently appeared as the first or second stimulus in any series o f paired trials, T h r o u g h o u t all trials, we attempted to ensure that the experimental protocol mimicked natural conditions as m u c h as possible. Vervets frequently foraged in dense bush near waterholcs or in shrubs and vines at the base o f tree, and they often grunted to one another when they were apparently out o f sight of each other. We therefore felt justified in assuming that a grunt played from a speaker, as if uttered by a monkey behind a bush or trees, was not anomalous.
Table I. Experimental Design
Stimuli tested Series 1 Grunt to subordinate Grunt to dominant
Series 2 Grunt to dominant male Grunt to dominant female
Series3 Grunt to dominant MIO grunt (see text)
Series 4 Grunt to dominant Grunt to another group
Series 5 MIO grunt (see text) Grunt to another group
743
Vocalizers
Subjects
Adult female DN (group A)
6 group A animals, all subordinate to DN
Adult female TD (group C)
6 group C animals, all subordinate to TD
Juvenile female LS (group A)
3 group A males (see text)
Adult female TD (group C)
3 group C males (see text)
Juvenile male DS (group A) Adult female DU (group B) Adult female TD (group C)
6 group B animals
6 group A animals
6 group C animals
Adult female DU (group B) Adult female TD (group C) Juvenile female C Y (group C)
6 group B animals 6 group C animals
Adult female DU (group B)
6 group B animals
Adult female TD (group C)
6 group C animals
6 group C animals
744
ANIMAL
BEHAVIOUR,
Eighty-six per cent of all trials involved a single subject. Exceptions occurred when a second of our predesignated subjects entered the playback area just as a trial began, and unavoidably heard the playback stimulus. In each trial, the subject was filmed with a sound movie camera (Elmo 350SL), for 10 s before and 10 s after the grunt was played. This procedure allowed us to record the grunt on the film sound track, to establish a baseline probability that the subject would show a given behaviour in the absence of a call, and to compare baseline data with the subject's behaviour after playback. A playback experiment was possible on only 10 to 2 0 ~ of all occasions when we prepared to conduct a trial. Attempts to conduct a trial were frustrated when, for example, the predesignated subject moved in an unanticipated direction, away from our chosen location, or when the subject concealed itself in a dense bush. Alternatively, the subject situated itself satisfactorily, but the individual whose grunt was about to be played emerged in full view. In all such cases, the trial was terminated before the grunt was broadcast. Data presented below are drawn from those instances in which a grunt was played and a complete film record obtained. In all playback trials, the movie camera was positioned at either 0, 90, 180, or 270* with respect to both the speaker and the subject. The monkeys' habituation to observers carrying equipment permitted rapid adjustment of the camera's position, and allowed us to control the angle at which trials were filmed. This procedure not only simplified film analysis, but also ensured that we could determine whether or not playbacks caused subjects to orient toward or away from the speaker. The data from each trial consisted of the film record, a narrative commentary spoken into a tape recorder during each trial, and a map drawn to include the position, identity and orientation of the subject, all nearby monkeys, vegetation, the speaker, the movie camera, and the observers. The map also included data on the location, orientation, and behaviour of the individual whose grunt was being played. In scoring the filmed responses to playback, we searched for either qualitative or quantitative differences in the monkeys' responses to different grunts. Responses were defined as follows: Move toward/away from the speaker. These responses were usually unambiguous on film. The minimum criterion for a move was two successive steps by the subject in the same direc-
30,
3
tion. If, however, the subject moved parallel to the speaker, so that it approached the speaker before moving away from it, we did not score the subject's response as a move away from the speaker. Scanning. This behaviour fell into four categories: (a) look toward the speaker; (b) look in the direction the speaker was pointed; (c) look in any other direction; (d) look at other monkeys. Animals were scored as having looked in the direction the speaker was pointed when a head movement oriented their gaze along a line parallel to the orientation o f the speaker (for definition of 'looks' see Cheney & Seyfarth 1980; Seyfarth et al. 1980a). A monkey could look at other monkeys at the same time that it looked in a given direction. When a monkey looked at others, their identities were recorded. Two measures were used in scoring films. Latency to respond to a grunt was measured by counting the number of frames from the onset of a grunt on the film sound track to the first indication that a subject began to show a given response. Duration was calculated (see below) using the number of frames, up to a maximum of 180 (10 s), during which a subject showed a given behaviour. Bout lengths were not distinguished in calculating duration (see Seyfarth et al. 1980a, page 1082). To correct for the subject's behaviour before playback, we defined duration of response as the duration of a given behaviour in the 10 s after playback minus the duration of the same behaviour in the 10 s before. Thus i f a subject looked toward the speaker for 36 frames (2 s) b e f o r e playback and for 108 frames (6 s) after playback, the duration of response was scored as 72 frames (4 s). In cases when playback produced no change in behaviour, duration of response was zero. When a subject showed more of a given behaviour before playback than after it, duration of response was scored as negative. Results Grunt to a subordinate versus grunt to a dominant. Six subjects in group A and six subjects
in group C were played grunts that had originally been recorded either as the vocalizer approached a subordinate female or as the vocalizer approached a dominant male (for data on subjects and vocalizers, see Table I). All 12 individuals in both groups were subordinate to the animal whose grunt was being played. In each group, three subjects heard the grunt to a subordinate first, and three subjects heard the
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS grunt to a dominant first. Overall, trials were conducted in a variety of social and environmental circumstances. Playback of grunts produced two kinds of responses: subjects either moved away from the speaker or looked toward the speaker for a longer period following playback than before. Significantly more subjects moved away from the speaker when hearing the grunt to a subordinate than when hearing the grunt to a dominant (Table II). For nine of 12 subjects, the duration of moving away and/or looking toward the speaker was greater following the grunt to a subordinate as opposed to the grunt to a dominant (N = 12, one tie, two-tailed binomial test, P = 0.066). There was no indication that subjects of different ranks responded differently to playbacks of each grunt type. Overall, the grunt to a subordinate evoked both a stronger and a qualitatively different response than the grunt to a dominant, suggesting that the two calls conveyed consistently different information. As mentioned above (see Methods), we attempted to conduct all trials at a time when, to the best of our knowledge, subjects were out of sight of the individual whose call was being played. Nevertheless, it might be argued that differences in the response to each grunt type occurred not because each grunt conveyed different information, but because the location of the original vocalizer was consistently different for each grunt type. With this in mind, we examined our records, but found no evidence that playbacks increased the probability that subjects would look toward the individual whose call was being played. Grunt to a dominant male versus grunt to a dominant female. The difference in the responses
of subjects to grunts given to a subordinate and grunts given to a dominant may have resulted in part because, regardless of the relative ranks of the animals involved, one grunt was originally given to a female while the other was originally Table H. Responses to Playback of Grunt to Subordinate and Grunt to Dominant
Move away from speaker after playback Yes
No
Grunt to subordinate
5
7
Grunt to dominant
0
12
Fisher Exact Probability Test (two-tailed), P < 0.05.
745
given to a male. In order to determine whether vocalizers gave different grunts to dominant animals depending upon those animals' sex, we designed a second series of experiments. In this series, six adult males (three from group A, three from group C) were played grunts that had originally been given by a female member of their group either as she approached a dominant male or as she approached a dominant female (Table I). All six subjects were subordinate to the male but dominant to the female. We reasoned that, if a vocalizer gave different grunts to dominant animals depending on their sex, subjects should respond more strongly to the grunt given to the male than to the grunt given to the female. Playback of the two grunt types produced one consistent response: subjects looked toward the speaker for a longer time following playback than before. There was no significant difference, however, between the two grunts in the duration that subjects looked toward the speaker (MannWhitney U-test, N1 = 6, N~ = 6, U = 17.5, P > 0.10). Results suggested that, when giving grunts to dominant animals, vervets did not distinguish between males and females. Grunt to a dominant versus grunt to an animal moving into an open area ( M I O ) . In our third
series of trials, six subjects in each of the three study groups were played grunts that had originally been given by a member o f their group either as it approached a dominant or as it watched another monkey move into an open area (MIO). As before, the order of stimulus presentation, as well as the location of the speaker relative to subjects, were varied throughout all trials (Table I). Results gave no indication that playbacks caused subjects to look at the individual whose call was being played. There were consistent differences, however, in the responses evoked by the two grunts. When compared with the MIO grunt, playback of grunts to a dominant produced significantly longer durations of looking toward the speaker (Fig. 2). The subjects again behaved as if the two grunts conveyed consistently different information. Grunt to a dominant versus grunt to another group. Six subjects in group B and 12 subjects
in group C were played grunts that had originally been given by a member of their group either as it approached a dominant or as it looked at another group (Table I). In these trials, grunts to another group produced significantly longer durations of looking in the direction the
ANIMAL
746
BEHAVIOUR,
speaker was pointed than did grunts to a dominant (Fig. 3). It should be emphasized ~hat the response of looking in the direction the speaker was pointed did not occur because subjects looked toward the animal whose call was being played. More-
40.
p<.O5
Grunt To: Dominant [ ]
~q
[]
MIO
i
20_
L
E
x
-2o_
n,-
.~
-4o
121
Look Toward
Look In Direction
Speaker
Speaker Is Pointed
Fig. 2. D u r a t i o n o f responses to playback of g r u n t to d o m i n a n t a n d M I O grunt. Y-axis s h o w s d u r a t i o n o f res p o n s e (defined in text), m e a s u r e d in frames of films at 18 fps. H i s t o g r a m s show m e a n s plus s t a n d a r d errors for subjects. Probability value based o n two-tailed M a n n W h i t n e y UXtest. L o o k toward speaker: N~ = 18, N2 = 18, U = 100, P < 0.05. L o o k in direction speaker is pointed: U = 137, P > 0.10.
40o
g =0
-~-
_1_
GruntTo: Dominant
3
over, the response was not simply due to an increase in scanning behaviour, since neither grunt significantly increased the duration of looking in directions other than the one in which the speaker was pointed. This is not to say that our data indicated the precise point toward which animals were looking. The film analysis permitted us to specify only four directions of orientation (see Methods). In summary, therefore, grunts to another group seemed to serve a rather specific 'alerting' function, directing the listener's attention away from the vocalizer and toward the area in which the vocalizer would ordinarily have been facing. M I O grunt versus grunt to another group. Finally, we compared the responses of six subjects in group B and six subjects in group C to the MIO grunt and the grunt to another group (Table I). In previous trials, these two grunts had elicited similar responses. Both produced a a slight increase in the duration of looking toward the speaker, as well as a slight increase in the duration of looking in the direction the speaker was pointed (Figs 2, 3). Thus it was not surprising to find no difference in the duration of responses elicited when the two calls were compared directly (Fig. 4). Nevertheless, other evidence suggested that the grunts evoked measurably different responses. Grunts to another group showed a shorter latency to elicit looking in the direction the speaker was pointed, while MIO grunts showed
[]
Other Group ll~ p< .05
2o
30,
|
3
Grunt To: MIO 40_
[]
Other Group 9
:m r
8
E.
20_
g
-zo-
E
&
g~
.~
-20-
-40 g Look Toward
Look
{n Direction
Speaker
Speaker Is Pointed
Fig. 3. D u r a t i o n o f responses to playback o f g r u n t to d o m i n a n t a n d g r u n t to a n o t h e r group. Legend as in Fig. 2. L o o k toward speaker: N t = 18, N~ = 17, U = 111.5, P > 0.10. L o o k in direction speaker is pointed: U -- 91, P < 0.05.
g
-40 Look
Toward
Speaker
Look In Direction
Speaker Is Pointed
Fig. 4. D u r a t i o n o f responses to p l a y b a c k o f M I O a n d g r u n t to a n o t h e r group. L e g e n d as in Fig. 2. toward speaker: N1 = 12, N2 = 11, U = 47.5, P > L o o k in direction speaker is pointed: U = 42, P >
grunt Look 0.10. 0.10.
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS a shorter latency to elicit looking ~ the speaker (Fig. 5). While each of these differences only approached significance (P < 0.07), they represented changes in two opposing behaviourai measures. Moreover, no other comparisons of different grunt types revealed any differences in the latency to elicit a given response. While not statistically significant, the M I O grunt and the grunt to another, group appeared to differ in their ability to produce a particular response, suggesting that the two calls may have conveyed different information to the monkeys. Part Two In experiments described in Part One, the responses'of subjects suggested that vervet monkeys distinguished among at least four different grunt types. Even to an experienced human listener, however, there were no immediately salient acoustical distinctions among the various grunt types. Subsequent laboratory analysis was therefore conducted to determine what acoustical cues might have been used by vervets to distinguish among different grunts. Methods
In order to conduct an accurate statistical analysis of the acoustical variants within and Grunt To: MIO P<.07
[]
Other Group I[~ p< ,07
150-
g$ I00-.
g
m
50-
#
Look Toward Speaker
Look in Direction Speaker Is Pointed
Fig. 5. Latency of subjects to respond to MIO grunt and grunt to another group. Y-axis shows latency to respond, measured in number of fraraes of film at 18 fps. Otherwise legend as in Fig. 2. Look toward speaker: N1 = 12, N2 = 9, U = 27, P < 0.07. Look in direction speaker is pointed: N1 = 12, N2 = I0, U -~ 31, P < 0.07. Animals who were looking toward the speaker or in the direction the speaker was pointed at the onset of playback have been exclud from analysis.
747
between the four grunt types described earlier, we required high quality exemplars from a number o f individuals, each of whom had been taperecorded a number of times in each of the four different contexts. Only under these conditions was: it possible to compare the acoustical properties of grunts given in different social contexts while simultaneously controlling for individual variation (Lillehei & Snowdon 1978). Examination of field recordings made in 1977, 1978, and 1980 revealed six individuals (all adult females) for whom these requirements were met. For each of these individuals, we had between five and 10 recordings of grunts given in each of the four contexts described above. Analysis of the acoustical properties of grunts was conducted with tape at normal and 1/4 speed, using a Kay sonagraph model 7029A, with a wide (300 Hz) or narrow (45 Hz) band filter, the FL1 shaping selector, and a frequency scale of 80-8000 Hz. More detailed spectral information was obtained using the computer system described by Zoloth et al. (1980), where the 256-point fast F o u r i e r transform has a minimum frequency resolution of 76.9 Hz. Power spectra taken over the entire duration of the call allowed accurate assessment of overall frequency peaks, while spectra taken of the first, second, and final third of each call allowed t~s to measure frequency modulation. Analysis was conducted on calls that had been corrected for the 'presence of background noise. This correction was made by first taking a power spectrum of the call, including its background noise, then taking a power spectrum of the background noise alone in the 100 ms preceding the call, and finally subtracting the latter from the former using the noise correction formula described by Peterson & Gross (t978). In the following section, the terms unit and call are defined as in Struhsaker (!967). As a first step in the acoustical analysis of grunt types, we examined the grunts given by one female (TD of group C) in the four contexts described above: when approaching a dominant, when approaching a subordinate, when watching another animal move into an open area (MIO), and when looking at another group. Sixteen acoustical features were measured. For each measure, an overall statistical test (either Chi-square or one-way analysis of variance) was used to determine the degree o f heterogeneity across call types. I f an acoustical feature showed significant heterogeneity across grunt types, we concluded that monkeys might potentially make
748
ANIMAL
BEHAVIOUR,
use o f the feature when distinguishing a m o n g grunts. As a second step in o u r analysis, we r e p e a t e d these tests using grunts f r o m five o t h e r a d u l t females: A P (group C), M P , D N , a n d LB (group A ) ; a n d D U (group B). Vocalizations f r o m each i n d i v i d u a l were analysed separately, following the p r o c e d u r e originally d e v e l o p e d for T D ' s grunts. Results
A s described above, we b e g a n by a n a l y s i n g the grunts o f one a d u l t female, T D . T h e m e a -
30,
3
sures tested, statistical tests used, a n d results are shown in T a b l e I I I (left-hand column). T a b l e I I I also s u m m a r i z e s the results o f similar analyses p e r f o r m e d on the five other females (righth a n d column). These results a r e described in greater detail below. T D ' s grunts, as well as those o f o t h e r vervet m o n k e y s , a p p e a r e d on a frequency versus time d i s p l a y as r a t h e r noisy, n o n - t o n a l sounds (Fig. 1 ; see also S t r u h s a k e r 1967, plate 16). N e v e r t h e less, detailed analysis revealed a n u m b e r o f acoustical measures t h a t c o u l d p o t e n t i a l l y a l l o w a listener to distinguish a m o n g grunts given in
Table HI. The Acoustical Features that Differentiated among Grunts Given by Adult Female TD (Left Columns) and Five Other Adult Females (Right Column) in Four Different Contexts
Adult female TD Acoustical feature tested
Test used
Result
Also significant for:
1. 2.
Call length Peak frequency
Anova Anova
P < 0.01 P < 0.01
LB AP, MP, DN, LB
3.
Amplitude difference between peaks
Anova
P < 0.01
AP, MP, DN, LB
4.
Presence/absence of 3rd frequency peak within 5 dB of strongest peak
X2
P < 0.01
5.
Frequency modulation of amplitude peak ~< 500 Hz
X~
NS
6.
Frequency modulation of amplitude peak between 500 and 1500 Hz
Z~
P < 0.05
7.
Number of units/call
Anova
P < 0.01
8.
Number of calls with amplitude peak in 1st unit
X2
NS
9.
Number of units with amplitude peak in 1st half
X2
NS
10.
Number of calls where unit with peak amplitude has amplitude peak in 1st half
X~
NS
11.
Unit length
Anova
P < 0.01
12.
Inter-unit interval
Anova
NS
13.
Pulse rate
Anova
NS
14.
Frequency of amplitude peak between 500 and 1500 Hz
Anova
NS
15.
Frequency separation between adjacent peaks
Anova
NS
16.
Changes in pulse rate within units over time
X~
P < 0.01
All probability values are two-tailed. NS
=
P > 0.10.
AP, MP, DN, DU
AP, DU, LB AP
AP, DN, LB
CHENEY & SEYFARTH: VERVET MONKEY VOCALIZATIONS different contexts. TD's grunt to a dominant, for example, contained o n e frequency peak, usually around 310 Hz. Grunts to a subordinate, MIO grunts, and grunts to another group contained a second peak, usually between 690 and 1500 Hz. In grunts to a subordinate the two peaks were of roughly equal amplitude. In M I O grunts the lower peak was stronger, while in grunts to another group the upper peak was stronger (Fig. 6; measures 2 and 3 in Table III). Each of these measures showed significant heterogeneity across grunt types (Table III), suggesting that these acoustical parameters could have been used to distinguish among TD's grunts. Additional analysis revealed a number of other parameters that distinguished TD's different grunt types. The MIO grunt was significantly more likely than all others to have an upper frequency peak that rose from the first to the second and fi'om the second to the final third of each call (measure 6, Table III). In grunts to a dominant and grunts to a subordinate, pulse rate generally decreased within each unit (see Fig. 1), while pulse rate increased or remained constant in M I O grunts and grunts to another group (measure 16, Table III). In order to determine whether the acoustical parameters t h a t permitted us to distinguish among TD's grunts remained constant across individuals, a second sample of recordings from five other adult females was analysed as outlined above. Of the 16 measures tested, seven
-Io
-20
In, 0
io
(b)
- o
1.0
2.0
:-. 0
1.0
749
were non,significant across grunt types for all five females, and three others were significant for only one female (Table III), Two measures showed significant differences for four females, and three were significant for five females. For at least some acoustical measures, therefore, there were consistent differences among individual grunt types, both across individuals and across groups. Precisely which of these acoustical distinctions were actually used by the monkeys remains to be determined. A more detailed analysis o f the different grunt types is currently in progress. The preliminary results described here, however, indicate two points of interest. First, some acoustical features were more likely than others to show heterogeneity across g r u n t types. Second, there was considerable 'agreement" among adult females in the acoustical cues that distinguished among different grunts. Discussion
The results of the field playback experiments are summarized in Table IV. In examining this table, it should be remembered that grunts to a subordinate were the only grunts tested that elicited movement away from the speaker (Table II). Thus although grunts to a subordinate were only compared directly against grunts to a dominant, there was indirect evidence that the monkeys would also distinguish grunts to a subordinate from M I O grunts and grunts to another group. Similarly, responses elicited by grunts to a dominant, MIO grunts, and grunts to another group could all be distinguished from one another by at least one behavioural Table IV. A Summary of Significant Differences between the Responses Evoked by Different Grunts
2.0
Grunt to:
Frequency (kHz)
Another
E
Subordinate Dominant MIO Subordinate Dominant -20
, 0
1.0
- 20
9 ~ 2.0
[
j:
0
I.(3
MIO
1
group
(Not tested) 2
4 (3), (5)
210
Frequency (kHz)
Fig. 6. Power spectra of four grunts given by the same individual (adult female TD) (a) when approaching a dominant, (b) when approaching a subordinate, (c) when watching another animal move into an open area (MIO), and (d) when looking at another group. Power spectra have been corrected for background noise (see text).
Measures tested were: (1) move away from the speaker; (2) duration of looking toward the speaker; (3) latency to look toward the speaker; (4) duration of looking in the direction speaker pointed; (5) latency to look in the direction speaker pointed. Entries in each cell indicate a significant difference at the 0.05 level. Entries in parerstheses indicate a level of significance of 0.07. All tests are two-tailed.
750
ANIMAL
BEHAVIOUR,
measure. Results suggest that each grunt type, like each of the vervets' alarm calls (Seyfarth et al. 1980a), transmits different and specific information. In this respect, the grunts appear to function in a rudimentary representational manner. Despite such outward similarities, however, the vervets' grunts are in many respects more subtle than their alarm calls. Alarm calls, for example, are easily distinguished by the human ear, whereas even a practised listener finds it difficult to tell one grunt type from another. Preliminary acoustical analysis has revealed a number of measures by which grunt types can potentially be distingushed from each other, but these measures are by no means as obvious as the acoustical distinctions among alarm calls. In an analogous manner, the alarm calls that vervets give to different predators evoke easily observable, qualitatively different responses from other monkeys (Seyfarth et al. 1980a), while the different responses evoked by different grunt types are much less easily distinguished. Distinctions among responses to different grunt types in playback trials were generally quantitative rather than qualitative: subjects showed more of a given response, or responded more quickly, when hearing one grunt type as opposed to another. Although only five grunt types were used as experimental stimuli, there is no reason to believe that the diversity of vervet grunts is restricted to the exemplars discussed here. Results of playback experiments support the hypothesis that the vocal repertoire of non-human primates, when assessed by the primates themselves, may be f a r larger than classification by human ear would suggest (see also Green 1975; Zoloth et al. 1979). There is s o m e evidence, then, that vervet monkey grunts transmit specific information, and that in some cases they may act as if they refer to external objects or events, such as another group, or a monkey moving into an open area. Do vervet grunts therefore resemble human words, so that when a monkey grunts it has a mental representation of some object or concept that it wishes to communicate (see e.g. SavageRumbaugh et al. 1980) ? Clearly, our data cannot address this question, since the experiments measured only the responses evoked by each grunt type. Such responses revealed nothing about the vocalizer's internal representation of interactions or objects. Nevertheless, the consistent differences in responses to each grunt type
30,
3
suggest that each grunt transmitted different infbrmation to the monkeys, without requiring full support of contextual cues (see also Premack 1973, 1975). This is not to say that contextual variables (including the vocalizer's own behaviour) are irrelevant in determining the 'meaning' of a grunt to other monkeys. Contextual components are doubtless important for the interpretation of grunts by vervets, just as contextual cues enrich the meaning of words for humans. Experiments suggest, however, that in many cases monkeys make less use of contextual cues than they do of acoustical features when interpreting the 'meaning' of a call. Although the playback experiments described here suggest that vervet monkeys may be capable of rudimentary representational signalling, they do not explain why natural selection might have favoured the use of such signals during social interactions. While it is not difficult to imagine the advantage of developing different alarm calls for predators with different modes of hunting, the benefits of such representational signalling within the group are less clear. The social environment within groups of Old World monkeys demands that individuals be able to make complex classifications of the bonds and relationships of other group members, and act adaptively on the basis of their extrapolations (Humphrey 1976; Seyfarth & Cheney, in press). It seems possible that the evolution of complex signal forms may have been favoured by the selective pressures placed on individuals by their fellow group members. The use of different calls in different contexts involves not only a reduction of uncertainty and ambiguity, but also an increase in the amount of information that can be conveyed to (or withheld from) others. Only by studying vocalizations within the broader context of other forms of social interactions, and by considering what primates need to signal about, will it be possible to begin to understand the selective forces that might have favoured the evolution of representational signalling.
Acknowledgments We thank the Office of the President and the Ministry of Tourism and Wildlife of the Republic of Kenya for permission to work in Amboseli National Park. We are especially grateful to B. Oguya, the Warden of Amboseli during this research project, for his kind assistance and cooperation. S. Green, S. Gilmore, H. and S.
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