Responses to context- and individual-specific cues in cotton-top tamarin long calls

Anim. Behav., 1983, 31, 92-101

RESPONSES TO CONTEXT- AND INDIVIDUAL-SPECIFIC CUES IN COTTON-TOP TAMARIN LONG CALLS

BY CHARLES T. SNOWDON, JAYNE CLEVELAND & JEFFREY A. FRENCH Department of Psychology, University of Wisconsin, Madison, Wisconsin 53706, U.S.A.

Abstract. We identified two variants of cotton-top tamarin long calls that occur in different situations: communication between troops and intratroop calling. A discriminant analysis differentiated between the forms of the two variants with a classification accuracy of 98 ~. Discriminant analyses and analyses of variance also differentiated between the call structures of individual animals for each type of long call. A playback experiment elicited alerting, arousal and aggressive responses only to the calls of non- troop members. Aggressive behaviour patterns were elicited by the intertroop long call variant (Normal Long Call) and not by the within troop variant (Quiet Long Call). The long call variants are perceived as different by the monkeys and elicit functionally different responses. Several parallels exist between the long calls of tamarins and the song of birds.

Introduction Many species of primates are noted for having some striking, attention-eliciting vocalizations within their repertoires: the howling of howler monkeys (Alouatta), the 'morning song' of the gibbons (Hylobates), the 'pant-hoot' of chimpanzees (Pan), the 'whoopgobble' of mangabeys (Cercocebus), and so on. These vocalizations have generally been called 'Loud Calls' by investigators of Old World primates (Gautier & Gautier 1977; Waser 1977) and 'Long Calls' by investigators of New World Primates (Moynihan 1970; Moody & Menzel 1976; Cleveland & Snowdon 1982). Whatever the label these vocalizations are loud, long, and highly con- spicuous.

A general consensus exists that there are three separate uses of these calls. First, loud or long calls are often given by territorial species with the effect of eliciting similar calls either from neighbouring animals or from other groups of animals moving away from the calling animal (Deputte 1982; Gautier & Gautier 1977; Waser 1977). In this context the call functions as a spacing signal, keeping different groups of animals apart from one another. Second, loud or long calls are often given by animals moving throughout their home range or after an ex- ternal disturbance; it seems to maintain contact or cohesion within a group (Moynihan 1970; Cleveland & Snowdon 1982). Third, long or loud calls are frequently observed in animals that have become separated from the rest of the group, eliciting calling from the other animals and movement toward the separated animal to restore contact (Waser 1977; Snowdon & Hodun, unpublished data). Solitary animals have a!so

been observed calling until joined by a potential mate (Moynihan 1970).

In recent years several reports have documented that calls which seemed to have only a very general function in fact have several variations, each of which is specific to a single context. The first demonstration was Green's (1975) study on Japanese macaques (Macaca fuscata), where seven variations of 'coo' vocalizations were found to occur in 10 different social contexts. There was a significant correlation between a specific variant and a specific social situation. Subsequently, other investigators have reported that variants in call structure are correlated with different contexts (Gautier 1974, for talapoins (Miopithecus talapoin); Lillehei & Snowdon 1978, for stumptail macaques (Macaca arctoides); Snowdon & Pola 1978, for pygmy marmosets (Cebuella pygmaea); Cleveland & Snowdon 1982, for cotton-top tamarins (Saguinus oedipus); Struhsaker 1967, and Seyfarth et al. 1980, f o r vervet monkeys ( Cercopithecus aethiops)).

Recent studies have also shown that there are individual differences in the structure of primate vocalizations, and that primates can recognize one another on the basis of these vocal differences. Marler & Hobbett (1975) showed individual differences in the call structure of chimpanzees (Pan troglodytes); Symmes et al. (1979) and Smith et al. (1982), have shown individual differences in the isolation peep and the chuck call of squirrel monkeys (Saimiri sciureus). Waser (1977) demonstrated individual differences in structure and individual recognition in the 'whoopgobble' display of grey-cheeked mangabeys (Cercocebus albigena); Cheney & Seyfarth (1980) demonstrated individual differences and

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SNOWDON ET AL.: RESPONSES TO TAMARIN LONG CALLS 93

individual recognition in the vervet (Cercopi- thecus aethiops); and Snowdon & Cleveland (1980) demonstrated individual differences and individual recognition in the calls of the pygmy marmoset ( Cebuella pygmaea).

Since monkeys often avoid long or loud calling animals of strange groups and approach loud or long calling animals of their own group, it seems logical that individual specific features would be incorporated into the structure of these calls. Since there is abundant evidence that context-specific call variants are found in several primate species, it also seems likely that animals would emit different variants of loud or long calls in different contexts. A recent study on the vocal repertoire of the cotton-top tamarin (Saguinus oedipus) by Cleveland & Snowdon (1982) suggested that there are context-specific long call variants in this species. Three types of long call (Fig. 1, Plate I) were described. The Normal Long Call appeared to be given primarily in response to hearing calls from animals in other" groups (see also the field study of Neyman 1978). The Quiet Long Call was usually of much lower amplitude and appeared to be used in intragroup communication only, often when animals were huddling, stationary or engaged in slow movement. It usually elicited chorusing from other group members. Both of these long calls consisted of a series of two or more whistles. The Combination Long Call consisted of several short syllables or chirps followed by whistle segments. The presence of short syllables or chirps was used to define the Combination Long Call as distinct from the other forms. Combination Long Calls were given by young animals when isolated from the rest of the group, by distressed animals within a group, and were the exclusive form of long call given by pre- adolescent animals (Thfirw~ichter 1980; Cleve- land & Snowdon, unpublished data). Combina- tion Long Calls are by definition acoustically different from the other long calls and are currently the subject of extensive research and thus are not considered further in the present report.

The present study examined two variants of long calls (the Quiet and Normal Long Calls) that are associated with different contexts in the cotton-top tamarin. Structural parameters were measured on a large sample of Normal and Quiet Long Calls and a discrinfinant analysis was performed to see if a classification function could be derived to separate the calls. Parameters were then measured for individuals' calls of

each type and subjected to discriminant analysis and multiple analyses of variance to determine if individuals could be differentiated on the basis of their long call structure. Finally, a playback study was conducted to evaluate the responses of cotton-top tamarins to each type of long call and to evaluate their responses to long calls of members of their own group versus calls of other group animals. The results indicate that the Normal and Quiet Long Calls can be differentiated, that individual differences exist in call structure, and that animals respond differently both to the particular form of long call played back and to the degree of familiarity of the individual whose long call is played back.

Animals Five mated pairs from a colony of cotton-top

tamarins ( Saguinus oedipus oedipus) were studied in this experiment. The original colony was obtained fl'om Professor Thelma Rowell at the University of California, Berkeley. Although the cotton-top tamarin is on the Endangered Species List, the animals in the colony were either born in captivity to legally-acquired animals, were obtained through breeding loans or trades of legally-acquired animals or were imported into the United States prior to the determination that they were an endangered species. They were housed in large home cages (minimum dimensions 2.5 x 1.75 x 2.35 m) con- structed of wood frames and hardware cloth walls. Small nest boxes, branches, and rope trails were provided for the animals' use. A 12h: 12h light: dark cycle was in effect with light onset occurring at approximately 0700 hours. The animals were fed a mixed diet of commercially prepared marmoset diet (Zu Preem Science Marmoset Diet), with daily supplements of fresh fruit, eggs, and vitamin C. Three of the groups consisted of an adult male, an adult female and from two to five offspring. The remaining two groups consisted of only an adult male and an adult female. One large room contained three home cages, while the other cages were located in individual rooms. Visual contact was eliminated between cages, but no attempt was made to preclude auditory or olfactory contact between cages.

Part 1 : Structural Analyses of Long Calls Method

Call selection. All calls were recorded from freely-behaving animals or from animals placed in situations designed to stimulate long calling.

94 A N I M A L B E H A V I O U R , 31, 1

Pilot studies showed that only mated adult animals gave Normal and Quiet Long Calls, hence all calls used for analysis and for subsequent playback were from mated adults. Calls were recorded by a Sennheiser MD441 microphone onto a Uher 4200 Report tape recorder at a speed of 9.5 cm/s.

Quiet Long Call/Normal Long Call differences. All clear spectrograms that could be measured accurately were used for statistical comparison (67 Normal Long Calls and 56 Quiet Long Calls). Four males and four females were represented in the Normal Long Call sample, and eight individuals (four males and four females) were represented in the Quiet Long Call sample. Each individual contributed from one to 16 calls to each of the long call samples.

Individual differences. Analyses of individual differences in both Quiet Long calls and Normal Long Calls were conducted only for animals for which we possessed a reasonably large sample of calls. Quiet Long calls from four animals (44 calls, 5 to 16 from each individual) and Normal Long Calls from five animals (62 calls, 9 to 16 from each individual) were analysed.

A sound spectrogram was produced for each call. A Model 6061B Kay Sound Spectrograph (Kay Elemetrics) set at 160 to 16 000 Hz with a narrow band (90 Hz) filter setting was used to produce the spectrograms.

Call measurement. Call frequency and duration parameters were measured by placing a ruled acetate graticule over the spectrogram. Duration measures were accurate to the nearest 25 ms and frequency measures were accurate to the nearest 0.25 kHz. One of us (JC) was respon- sible for all call measurements. Both types of long calls typically consisted of one to four long whistles (see Fig. 1). Parameters included the duration of the first and last whistle segment, and the frequency at the beginning and end as well as the change in frequency across the segment for the first and last whistle in each call. The number of whistle segments in each call was also noted. Accurate measurements of absolute amplitude could not be made since head position and distance from the microphone cannot be controlled in recording from freely moving monkeys.

Analysis. The data were analysed using the BMDP-7M Discriminant Function Program (Dixson & Brown 1979). A hierarchical step- wise analysis was used. In that form of discriminant analysis, an F-ratio was calculated for

each variable. If an F value was 4.0 or greater, the variable was included in the analysis, The variable that contributed most to Mahalanobis D ~ measure (a relative measure of distance), and thus maximally discriminated between the types of calls or between calls of individuals, was the first variable chosen for analysis. New F-ratios were then computed, using the variable first chosen as a covariate, partialling out the effects of the correlation between the first variable with the others. The calculation of D ~ was then repeated, with the next variable chosen being the one that maximally discriminated between the groups. These calculations continued until either all variables were used in the analysis or the F-ratios for the remaining variables were less than 4.0.

The accuracy or validity of the generated discriminant functions were assessed by a jack- knifed procedure. In this procedure discriminant functions are generated on N--1 of the items in the sample. These functions are then used to predict group membership of the item eliminated from the calculations. This procedure is repeated N times, successively eliminating each item from the calculation of the discriminant functions. The jack-knifed validation procedure has the advantage of not including the item to be classified in the generation of the discriminant function used to classify that item.

Since there were some F-ratios that were significant but were less than 4.0 and thus eliminated from the discriminant analyses, in the analyses of individual differences an analysis of variance was performed on each variable that had a significant F-ratio. Tukey's HSD test was applied to determine which individual means were significantly different from other individual means for each variable. These results were then cast into a table of distinctive features.

Results Differentiation of long call structures. The

discriminant analysis of the two types of long calls identified several parameters on which they could be differentiated. Table I presents the group means and standard deviations for the major parameters of the population of long calls identified according to situation. In general the results replicated those of Cleveland & Snowdon (1982), showing that the Quiet Long Call was characterized by shorter duration of the first and final syllables, by a greater frequency range or frequency modulation in each of the

SNOWDON ET AL.: RESPONSES TO TAMARIN LONG CALLS

Table I. Means, Standard Deviations and Diserhn~nant Function Coefficients for Parameters Differentiating Long Calls

95

Group means + (so) Discriminant function

coefficients

Quiet Normal Quiet Normal Long Call Long Calt F to enter Long Call Long Call

First syllable duration 477.70 1130.91 279.59 (ms) (248.89) (183.64)

Last syllable duration 705.37 1032.48 25.52 (ms) (252.66) (196.16)

First syllable frequency change 0.33 0.22 28.66 (kHz) (0.53) (0.22)

Last syllable frequency change t.15 0.38 9.29 (kHz) (0.53) (0.17)

No. of syllables 2.07 2.55 5.46 (0.42) (0.61)

First syllable start frequency 1.09 1.04 3.25 (kHz) (0.45) (0.28)

Last syllable start frequency 1.33 1.19 3.86 (kHz) (0.34) (0.18)

Constants

0.009 0.024

0.015 0.023

2.150 -2.998

6.632 1.218

7.816 9.729

-20.501 -38.710

syllables measured, and by fewer syllables. The start frequencies of each syllable did not differ between the two calls. The discriminant function coefficients presented in Table I should provide a successful prediction of subsequent Quiet or Normal long call types.

When the classification accuracy was tested using the discriminant function, 121 of the 123 calls were correctly classified. When the jack- knifed validation matrix was examined, the classification accuracy was only slightly reduced to 119 of 123 calls classified correctly (see Table II). Thus, the two hypothesized forms of 10ng calls given in different situations are significantly different in their structures.

Differentiation of individual calls. The discriminant analyses of individual calls were less successful. In the analysis of the Quiet Long Call, with a sample from four individual animals, the success rate of the discriminant analysis was 68.2 %, weIl above the chance level of 25 %. The results showed there was substantial variability in the analysis, with the calls of two animals being correctly identified by the discriminant function with high frequency (87.5% (female) and 78.6% (male) correct respectively), one animal being correctly identified at 60%

(female) while another animal was correctly identified at chance level (22% (male) correct).

In the discriminant analysis, only one parameter, the first syllable duration, met the cri- terion of having an F-ratio of 4.0 or greater. However, last syllable frequency change had a significant F-ratio. Separate analyses of variance were carried out on these two variables. Sub- sequent Tukey HSD means tests indicated that the calls of the four animals could be well differentiated from one another using the two variables. The results are presented in Table III .

The results of the discriminant analysis on the Normal Long Calls of the five animals were similar. The calls were correctly classified 56.5 of the time which is considerably above the chance level of 20 %. Again there was a wide range of discriminant success. The calls of one animal (a female) were classified with an accuracy of 100%, while the rest of the animals' calls were classified correctly slightly less than 50 % (three females and one male) of the time. Only two parameters (first syllable start frequency and last syllable start frequency) were used in the discriminant analysis, the remainder having an F-ratio below 4.0. Last syllable duration also had a significant F-ratio and analyses of variance

96 A N I M A L B E H A V I O U R , 31 , 1

Table II. Classification Matrices for Normal and Jack-knifed Discriminant Validation

Classification matrix Jack-knifed validation matrix

Quiet Normal % Quiet Normal % Call group Long Call Long Call Correct Long Call Long Call Correct

Quiet Long Call 55 1 98.2 53 3 94.6 Normal Long Call 1 66 98.5 1 66 98.5 Total 56 67 98.4 54 69 96.7

Table III. IndMduai Differences in Quiet Long Calls (mean • (SD))

Animal

Parameter Kama Jason Euclid Kate

First syllable duration 5060 354- 652 + 850 ++ (ms) (91) (157) (249) (266)

Second syllable frequency 1.0- 1.6 + 0.8- 1.0- change (kHz) (0.2) (0.7) (0.7) (0.4)

Means with superscript + differ from means with superscript-, P < 0.05; means with superscript ++differ from means with superscripts-, 0 p < 0.05.

and the Tukey HSD test of differences between means on each of the three variables produced a distinct pat tern of individual differences as shown in Table IV.

Part 2: Playback of Normal and Quiet Long Calls

Method Stimuli. There were eight st imulus condit ions

in the playback study. Control stimuli consisted of two types. The first was a 3 to 5 s recording of background colony noise without any animal vocalizations. The second consisted of a b lank tape with no recorded noise. Three forms of Quiet Long Calls were presented: the test an imal ' s own calls; the test animal ' s mate 's calls; and calls of other animals from the colony.

Fou r types of Norma l Long Call stimuli were used: the test animal ' s own calls; the test animal ' s mate 's calls; calls f rom other animals f rom the colony; and calls from animals in a different colony that the test animals never had heard before. Several examples of each type of call were used so that animals would no t hear the identical stimuli on different trials, and equal numbers of calls from unfamil iar males and u n f a m i l i a r females were presented as stimuli.

Procedure. The stimuli were prerecorded on cassette tapes upon which a time signal had been recorded to denote 15-s intervals. Three stimuli were recorded on a tape at 10 min, 25 min and 40 min from the start of the tape. For

Table IV. Individual Differences in Normal Long Calls (mean ~ (SD))

AnimaI

Parameter Carlotta Euclid Kate Poco Martha

First syllable start frequency 0.9- 0.8- 1.0 ~ 1.2 + 1.4 ++ (kHz) (0.2) (0.1) (0.2) (0.2) (0.3)

Second syllable start frequency 1.10 1.0- 1.10 1.2 + 1.5 ++ (kHz) (0.2) (0.2) (0.1) (0.1) (0.0)

Second syllable duration 9400 9540 1127 + 1150 ++ 922- (ms) (244) (126) (t76) (130) (102~

Means with superscripts + differ from means with superscript-, P < 0.05; means with superscript ++ differ from means with superscript 0, -, p < 0.05.

SNOWDON ET AL. : RESPONSES TO TAMARIN LONG CALLS 97

each trial this provided a 5-min period for animals to recover from any response to the starting of the tape, a 5-rain pre-stimulus base- line condition, and a 5-rain post-stimulus condition. Observations of the animals were made during both the pre- and post-stimulus periods.

Stimuli were presented in a counterbalanced order to each of the five adult male-adult female pairs in their home cages with only three stimulus presentations being given within a day's session. Animals were tested no more than twice weekly. These constraints were based on our previous experience with auditory playbacks and served to minimize habituation to the playback stimuli. The speakers were hidden and placed at the same vertical level where the monkeys normally spent most of their time. These steps were taken to maximize the ecologi-

c a l validity of the playback technique. Tests were continued until each pair of animals had been presented with each of the eight stimulus conditions six t imes- -a total of 48 trials or 16 sessions.

Playback amplitude was adjusted to that of Normal Long Calls for all stimuli. During the test session two observers were used, each recording the behaviour of one of the two adult animals in the cage. The observers maintained a mean interobserver reliability of 89 ~ across all measures. Several activities were selected for scoring based on our previous observations of the responses to spontaneous use of calls in these animals (Cleveland & Snowdon 1982). Following Normal Long Calls, antiphonal long calls, scent marking, piloerection, and environmental scanning may be observed. Following Quiet Long Calls, antiphonal Quiet Long Calls, whistles, and environmental scanning (defined as an elevation of the head above the hori- zontal, a rotation of the head, and gaze direction outside of the cage) occur. Type E (Alarm)

Ch i rp s (Cleveland & Snowdon 1982) are given as startle responses and might be expected after either type of long call. Long calls and scent marks were scored in terms of absolute frequency of occurrence, while piloerection, scanning, and alarm calls were recorded using a one-zero scoring technique (Altmann 1974).

Data analyses. The data were summed for each pre-stimulus and post-stimulus observation for each stimulus type across the six replications for each animal. Change scores were then computed by subtracting the pre-stimulus values from the post-stimulus values. Preliminary analyses showed that there were no differences

in the response to the two control conditions (no sound and cage noise), so these were combined into a common 'null stimulus' category. There were also no differences in responses to one's own versus one's mate 's calls, so these were also combined into a common 'own group' category. Finally, there were no differences between the responses to calls of other non- group animals within the colony and to totally strange animals' calls, so these were combined into a common 'other group' category.

For the final data analysis, the post-pre- stimulus change scores from the 'null condition' were compared with the post-pre-stimulus change scores from the 'own group', and then with the change scores from the 'other group' conditions for each call type and each response measure. Significance was evaluated using both the t-test and the Wilcoxon test. Although the direction of change in scores was predicted a prio?i, two-tailed tests were used to determine significance.

Results There was a clear discrimination between the

calls of one's own group and the calls of animals from other groups. No response measure with either type of long call showed any significant change in response to the calls of one's own group compared with the responses on null trials (Ps > 0.10). On the other hand, there were clear response changes when the calls were from members of other groups. These responses differed as a function of the type of call played.

Scanning increased after the playbacks of both types of long calls from other g roup animals (t-test: QLC versus n u l l - 2.78, df--9 , P < 0.05; NLC versus null = 2.56, df= 9, P < 0.05). The results are illustrated in Fig. 2. Scent marking was observed at a higher rate following the presentation of other group Normal Long Calls ( t - - 2 . 1 6 , df= 9, P < 0.059). The two-tailed test approached significance; however, the change scores of scent marking following Quiet Long Calls decreased relative to null scores, while the scores following the other group's Normal Long calls increased. Scent marking is probably a response specific to hearing other group Normal Long Calls. Piloerection response measures were similar to those of scent marking: there was an increase approaching significance in piloerection following presentation of other group Normal Long Calls, but not following the presentation of other group Quiet Long Calls (t = 2.21, df = 9,


P = 0.054). Again the change scores following other group Quiet Long Calls decreased relative to the null stimulus, while change scores following other group Normal Long Calls increased indicating that piloerection is also probably specific to other group Normal Long Calls. The results are illustrated in Fig. 2.

Finally, Alarm Chirps were given with greater frequency following presentation of other group Quiet Long Calls than Normal Long Calls (t = 2.41, df--- 9, P < 0.05). The results are illustrated in Fig. 2.

There were not sufficient antiphonal long calls given in response to any of the long call playbacks to analyse statistically.

Discussion There are distinct variant forms of long calls

used by cotton-top tamarins. The Normal Long Call is given in response to hearing the calls of strange animals at a distance; the Quiet Long Call is used for within group cohesion and is rarely heard in response to the sounds of a strange group (Cleveland & Snowdon 1982). These calls are structurally differentiated on several acoustic parameters, and a discriminant function (which correctly identifies 98 ~ of the calls) can be used to differentiate subsequent long calls.

There were consistent individual differences in the calls. The discriminant analyses identified calls as belonging to a given individual at a level significantly greater than chance, and when all variables with significant F-ratios were analysed a unique set of distinctive features

Scan

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OTHER GROUP CALLS

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Fig. 2. Mean pre- to post-stimulus change scores for each behavioural category in response to null, other group Quiet Long Call, and other group Normal Long Call stimulus presentation. Vertical bars indicate standard error of the mean.

was found for each animal. Nonetheless, the analyses were not perfect in the assignment of calls to individuals. There are two reasons for this lack of perfection. First, rates of spontaneous long calls varied greatly among individuals, and we could not obtain equally large samples for each individual. With more samples, the likeli- hood of generating a more accurate discriminant function would be greater. Second, we measured seven frequency and duration parameters. Accurate measurements of absolute amplitude could not be obtained, and it is possible that amplitude and other parameters that we did not measure may be used by the monkeys in their identification of individuals.

It is interesting to note that two of the variables discriminating between individual Normal Long Calls (first syllable start frequency and second syllable start frequency) were the parameters that were not used in the discriminant function to differentiate between Quiet and Normal Long Calls. A similar finding that the parameters used to distinguish call variants used in different contexts differ from those used to distinguish the call variants of different individuals has been reported by Lillehei & Snowdon (1978) for stumptail macaques.

When both types of calls were presented to animals in a playback study, there was no change in responses to calls of familiar animals (oneself and one's mate) relative to responses given in a no-stimulus control condition, but there were changes in several responses to calls of other group animals. Thus, the animals were discriminating among the calls of individuals at least on a familiar-unfamiliar dimension. With the presentation of other group calls of both types, the animals showed a significant orienta- tion to the calls with increased scanning behaviour. Piloerection and scent marking behaviour normally seen in response to unfamiliar con'- specifics (French & Snowdon 1981) were given with increased frequency following playback of other group Normal Long Calls but not to other group Quiet Long Calls. On the other hand, there was an increase in Alarm Chirps to Quiet Long Calls but not to Normal Long Calls. The increase in Alarm Chirps, a startle response, to unfamiliar Quiet Long Calls might be because animals in the wild would not normally hear Quiet Long Calls from a strange group or because the amplitude of the Quiet Long Call had been adjusted to match that of the Normal Long Call for the playback tests. The animals could distinguish differences in call structure

SNOWDON ET AL. : RESPONSES TO TAMARIN LONG CALLS 99

and could respond differentially and appropri- ately to the type of long call presented. The individual differences that were determined to exist in the structural analysis of the calls may be the basis for the differentiation response to 'own group' versus 'other group' calls.

Field studies of this species (Neyman 1978) indicate Chat group sizes range from 4 to 13 animals and that members of one group may come into contact with up to four other groups. However contacts with another group occurred 'once every few days,' and only mated adult males and females within a group give these long calls. Hence the testing procedures used in this experiment (stimulus calls from four strange groups; tests no more than twice a week) closely mimic the discrimination task which the animals would be likely to encounter in the wild.

Several authors have described long or loud calls as having different functions. Marler (t968) distinguished between the aggregation and dispersal functions for these calls. Gautier & Gautier (1977), reviewing the loud calls of vervets and guenons, noted that the Type I loud call (analogous to the long calls studied in the cotton-top tamarin) had both an intragroup rallying function and served to maintain distance between groups. Waser (1982), reviewing loud calls in baboons and mangabeys, described three contexts in which the calls were given: (1) following a disturbance induced from outside the group either by a conspecific group or by a predator; (2) following other vocalizations within the group and thus possibly serving for group cohesion (Waser also noted that these loud calls were generally softer than those given in other contexts); and (3) following loss of contact with other group members. The general consensus of results on Old World primates is that loud calls appear "in all three contexts. However, there has as yet been no study which indicates separate variants of loud calls that are specific to each context.

Several studies of New World primates have reached the same conclusions. Moynihan (1970), studying the subspecies Saguinus oedipus geoffroyi concluded that long calls were used in four contexts: (1) intergroup calling; (2) lost animal calling; (3) the group's response to lost animals; and (4) unmated solitary animals whose calling continued at a high rate until a mate was found. Moynihan did not present evidence of different call structures associated with different contexts, but Moody & Menzel (1976), studying another tamarin species (Saguinus fitscicollis illigeri), did

describe two forms of long calls: (1) the long loud call that was used in distance exchange, and (2) the long soft call that was used as for group cohesion. They presented no spectrograms of the latter call, but it appears to be analogous to the softer loud calls reported by Waser (1982) for intragroup calling, and both are in turn analogous to the Quiet Long Call of the cotton-top tamarin that is used as an intragroup cohesion call.

The only species that has previously been shown to have different Ibrms of long calls which are used in different contexts is the tiff monkey (Calticebus moloch) (Robinson 1979, 1981). Three types of calls were labelled according to the form of the units comprising the call. The 'chirrup' and the 'chirrup-pant-pump' were given during boundary encounters when animals from separate groups were close together. When animals were presented with playbacks of each of these calls, they gave different responses. 'Chirrups' elicited other 'chirrups' as responses while 'chirrup-pant-pumps' elicited both 'chirrup- pant-pumps' and duetting responses between the mated animals. Thus, although the calls were used in similar situations, they were responded to differently by the titi monkeys. The 'chirrup- pumps' were given early in the morning when pairs of animals were in the centre of their territories and thus quite distant from neighbouring groups. Playbacks of these calls elicited antiphonal 'chirrup-pumps' and male calling. These results on tiff monkeys are parallel to those presented here, with different calls appear- ing in different contexts and playbacks of each type of call eliciting different responses.

Both Moynihan (1970) and Gautier & Gautier (1977) mention the similarities between long or loud calls in primates and bird song, which is also used for spacing between groups, rnaintaining intragroup cohesion, and for mate attraction by solitary animals. There have been relatively few studies that indicate different forms of bird song for each type of context in which song is given, though there is considerable documentation of song variation and repertoire size (Krebs & Kroodsma 1980). Ficken & Ficken (1970) reported two different types of songs in four species of warblers that elicited two different patterns of response during playback studies. Smith et al. (1978) demonstrated that certain variants of the songs of yellow- throated vireos (Vireo olivaceous) were correlated with different contexts. Similar to Robinson with tiff monkeys, Smith et al. found one type of


song used when the birds were close to their nests and thus far from neighbouring groups, and another type of song used at territorial boundaries when animals from different groups came into direct confrontation. Thus there is some similarity between the differentiation of song types for use in different contexts by birds and in the differentiation of long calls for use in different contexts by some primates.

One final parallel between primate long or loud calls and bird song is in individual recognition. Waser (1977) demonstrated that most mangabeys would approach a speaker playing back a loud call of one of their own group, but would avoid the speaker when the loud call of a strange animal was played back. The only exception to this was generally a single male in each group that would approach the source of a strange call while the rest of the group retreated. Gautier & Gautier (1977) have reported that they could identify individual differences in the long calls of guenons, and Marler & Hobbett (1975) demonstrated individual differences in the loud calls of chimpanzees. The present study demonstrated that monkeys had individually different long calls and that they responded only to the playbacks of strangers' long calls, and not to the playbacks of familiar calls.

Brooks & Falls (1975), with the white- throated sparrow (Zonotrichia albicollis); Falls & McNicholl (1979) for the blue grouse (Dendra- gapus obscurus); Searcy et al. (1981) for the swamp sparrow (Melospiza georgiana); and Wiley & Wiley (1977) for the stripe-backed wren (Campylorhynchus nuchalis), have all demonstrated familiar animal-strange animal discrimination on the basis of song playbacks.

Waser (1982) has argued that increasingly clear individual differences in loud calls appear as species become more forest living and more arboreal. It would seem that for some New World primates there may also be an increasing differentiation of long call structure to correlate with different contexts. In situations of low visibility, other modalities that might ordinarily provide contextual cues for animals are less available, and hence, context must become specified in the structure of the signal itself. It is interesting to note that those few bird species in which contextual differentiation in song variants has been documented live in canopies. If an animal can differentiate between subtle variations in call structure and can respond appro- priately to each variant, then context should be specified by the call rather than through other

means, in addition, any call system involved in intergroup avoidance and intragroup cohesion requires that members of one's own group can be discriminated from members of other groups. The results with cotton-top tamarins indicate that differences in structure exist between long calls given in different contexts and between the calls of different individuals. The monkeys can detect and respond to contextual variations and discriminate between own group and other group calls.

Acknowledgments All authors contributed equally to the study. This research was supported by a USPHS Grant MH 29775, and a Research Scientist Development Award MH 00177 to Charles T. Snowdon. We thank Dr Harriet J. Smith for supplying us with recordings of her cotton-top tamarin long calls and for her advice on the experimentation. We thank Kimberly Bauers, Alexandra Hodun and Patricia McConnell for their comments and criticisms of the manuscript.

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(Received 11 January 1982; revised 20 April 1982; MS. number A2777)

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Responses to context- and individual-specific cues in cotton-top tamarin long calls