American Journal of Primatology 8:205-213 (1985)

Troop-Specific Responses to Long Calls of Isolated Tarnarins (Saguinus mystax)

CHARLES T. SNOWDON AND ALEXANDRA HODUN Department of Psychology, University of Wisconsin, Madison

Recently captured moustached tamarins (Suguinus mystax) were briefly separated from other members of their troop. Most separated animals emit- ted long calls that were, in general, similar in acoustic structure to those of sympatric tamarin species while retaining species distinctiveness. Individ- ual differences also appeared in call structure. The long calls of a separated animal were responded to almost entirely by members of the animal’s own troop rather than by other troops, and reciprocal calling occurred among troop members significantly more often than expected by chance. Although there was no evidence of troop-specific call structure or dialect, there were troop-specific responses to the calls of separated tamarins. This response implies the existence of a stable and integrated troop structure that allows troop members to learn and to respond to the individual specific features of each troop member’s calls.

Key words: moustached tamarin, Suguinus mystax, long calls. separation, individual recognition, troop responding

INTRODUCTION The moustached tamarin (Suguinus mystax) has been used extensively in

biomedical research, especially in the development of a hepatitis A vaccine [Provost et al, 1978; Ebert et al, 19781, but little is known of its ecology and behavior in the wild. It is distributed in the Western Amazon basin, south of the Amazon River and east of the Rio Tapiche in eastern Peru, and west of the Rio Madeira in Brazil [Hershkovitz, 19771. Like most tamarin species, it lives in small social groups that defend territories and in which no more than one female is reproductively active [Garber et al, 1984; Soini & Soini, 19821. S. mystax is typically found in sympatry with the saddleback tamarin, Suguinus fuscicollis nigrifrons and S. f i fuscicollis. Recently Terborgh [1983] has documented that S. fiLscicollis and S. imperator (a close relative of S. mystcwc) forage together and defend a common territory against intruders of either species. There is some evidence of a similar relationship between S. mystax and S. fuscicollis [Castro & Soini, 1977; Soini & Soini, 19821.

A consistent finding across a wide range of primate species is that specific individual vocal features can be identified, and that these features can be used by

Received September 7, 1984; revision accepted November 28, 1984.

Address reprint requests to Charles T. Snowdon, Department of Psycholoby, University of Wisconsin, Madison. WI 53706.

0 1985 Alan R. T,iss, Tnc.

206 I Snowdon and Hodun

conspecifics for individual identification. The most commonly found evidence of vocal recognition has been between mothers and infants. For example, in squirrel mon- keys (Sazmiri sciureus), Symmes et a1 119791 demonstrated consistent individual features in the structure of infant isolation calls, and Kaplan et a1 119781 demon- strated that mothers could recognize infant squirrel monkeys on the basis of vocal cues alone. Recently Symmes and Biben (unpublished manuscript) have shown that this recognition of infants by mothers occurs specifically with the isolation peep vocalization. In Old World primates, Lillehei and Snowdon [1978] demonstrated that young stumptail macaques (Macaca arctoides) had individually distinctive “coo” vocalizations. Hansen [1976] found that young rhesus macaques (Macaca mulatta) responded selectively to the calls of their mothers. Cheney and Seyfarth 119801 showed that vervet monkey (Cercopithecus aethiops) females would respond selec- tively to auditory playbacks of the calls of their own infants.

Data from arboreal and territorial species like the moustached tamarin have shown that several or all members of a group recognize each other on the basis of vocal cues. Waser [ 19771, for example, has shown that gray-cheeked mangabeys (Cercocehus albigena) are able to recognize the vocal playback of the territorial call of the group’s dominant male. They approach the playback location when the call of their group’s dominant male is broadcast, but avoid the playback location if a male of another group’s call is broadcast. Snowdon and Cleveland [1980] have demon- strated that adult pygmy marmosets (Cebuella pygmaea) can recognize each other by voice alone.

In the cotton-top tamarin (Saguznus oedipus), a species related to the mous- tached tamarin, there appear to be at least two variants of the territorial long call [Cleveland & Snowdon, 19821: One, used for territorial defense, is given in response to hearing calls from an unfamiliar group; the other is given to promote cohesion within a group and by animals that have become separated from the rest of the group (McConnell & Snowdon, unpublished observation). Two long-call variants, possibly with similar functions, have been observed in saddleback tamarins (S. fuscicollzs) [Moody & Menzel, 19761. Responses of cotton-top tamarins to their two forms of long calls demonstrated individual discriminability. Snowdon et a1 [ 19831 presented pairs of cotton-top tamarins with playbacks of each type of long call, including long calls originally emitted by the members of the group being tested and calls by unfamiliar individuals. S. oedipus responded with increased aggressive behavior to playbacks of territorial long calls from other groups, and with increased alerting and arousal behavior to the playbacks of cohesive long calls from unfamiliar individuals. No such responses were given to playbacks of calls from members of the test group.

In the study reported here, the vocal responses of moustached tamarins (Sa- guinus mystax) were examined. Reactions to a brief separation of an individual from its troop members were studied in the field shortly after the capture of observed natural troops. We provide descriptions of the long-call vocalization of this tamarin species given in conditions of separation and discuss the frequency of long calls and the latency to long calling as a function of the age, sex, and reproductive status of the separated animals. Notably, the responses of other monkeys to the calls of a separated animal were almost entirely from the troop of the separated animal. Thus, the animals were able to discriminate between troop and nontroop members on the basis of the vocal cues in the long call given by a separated animal.

METHODS Subjects

The subjects were 27 moustached tamarins comprising all of the members of five natural troops. Table I presents the distribution of animals in age-sex classes

TroopSpecific Responses to S. mystax Calls I 207

TABLE I. Comuosition of Troous

Adult Breeding Nonbreeding Subadult Subadult Troop male female adult female male female

C 1 1 17 3 1 1 18 1 1 1 19 3 1 2 2 1 20 3 1 2 2 Total 10 5 4 5 3

for all troops. The animals were trapped along the east bank of the Rio Tapiche, south of the Rio Yanuyacu in northeastern Peru at approximately 74"W and 6"S, as part of a collaborative captive breeding program between the Republic of Peru and the Pan American Health Organization (Proyecto Primates, Iquitos, Peru). Animals were habituated to the traps for several days until all known members of a troop entered the open traps for food. Then an entire troop was captured at one time. Upon arrival a t camp, each animal was classified by sex, approximate age, and parity by P. Soini, the biologist in charge of the trapping. Age was estimated on the basis of dentition wear, body size, and suprapubic gland size and structure. Only one parous female was found in each troop, as is typical for this species [Soini & Soini, 19821.

Upon completion of the examination and prior to shipment to Iquitos, individu- als were housed in separate cages, but individuals from a given troop were housed in close proximity to one another. They could see, hear, smell, and, on occasion, touch each other.

Procedure With the exception of troop C, which had been in camp prior to our arrival, each

troop was tested within 3 days of capture. A test consisted of a 10-min session per animal on each of 2 consecutive days. Prior to a test, some troops were moved to a position 40 m from where all of the troops were normally housed. From this position the animals that had been moved could not see the remaining animals, although they could hear one another. On one trial the troop whose members were to be tested was moved to the location 40 m from the rest of the animals; on the other trial all of the other troops were relocated 40 m away while the troop to be tested remained in place. The order was counterbalanced across groups to minimize the effects of disturbance due to movement alone. This design reduced the likelihood that animals were responding to movement or the approach of the experimenters rather than to the individual's calls.

After an adaptation period to the relocation, an individual animal was moved in its cage away from its own troop and isolated at a position approximately midway between the two locations of animals and out of sight of each. A Sony TC-158 cassette recorder with a microphone with a flat frequency response up to 14 kHz was placed in front of the isolated animal to record all of its vocalizations during a test session. One observer sat in a location where the test animal and its home troop could be observed, and the other observer sat in a location where the test animal and the animals from the other troops could be observed. Whenever the isolated animal called, each observer recorded whether or not vocal responses were made by the animals helshe was observing.

Each animal was removed from the proximity of its home troop to the separation location for a 10-min period, during which time vocal recordings and observations were made. At the end of this period the animal was returned to the proximity of its troop, and another animal from that troop was tested.

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Data Analyses Upon return from the field, the recordings of animal vocalizations were dis-

played on a real-time spectrum analyzer (Spectral Dynamics 301 SD) to determine the number of long calls given in the 10-min session and the latency to the first long call. For each of these long calls we then determined from our field notes whether a vocal response had been given by either troop or nontroop animals within 15 sec of the call of the isolate animal. The percentages of long calls responded to by troop and nontroop animals were compared, and a correlated sample t-test was used to determine whether these percentages differed.

In a second analysis, all reciprocal calling between the separated animal and troop and nontroop animals was examined. Reciprocal calling included the long calls and other vocalizations of the separated animal which were responded to by other animals and the long calls and other vocalizations of other animals that were responded to by the separated animal. Separate tallies were made of reciprocal calling between the separated animal and its own troop and the separated animal and nontroop animals. For each individual tested, expected values for reciprocal calling were computed by multiplying the number of reciprocal calls observed by the proportion of troop members to all animals present and by the proportion of nontroop animals to all animals present. These expected values were then compared with the observed values for reciprocal calling between the subject and troop or nontroop members. A X2 test using Yates’s correction for continuity was used to determine if the observed distribution of responses differed significantly from a chance distribution.

Seven animals that displayed a high rate of long calling were selected for further analysis of the structure of long calls. Sound spectrograms of their long calls were made with a Kay model 6061 B Sound Spectrograph using the 160-16,000 Hz frequency range and a narrow band filter.

RESULTS Figure 1 presents typical sound spectrograms of long calls from seven animals.

The long calls were typically 2-3 sec in duration and consisted of 14-17 individual syllables. Over the entire call there was an upward intonation or increasing fre- quency with successive syllables. In the early syllables of thc call there was evidence of a downward frequency modulation at the end of each syllable, but this downsweep became progressively less pronounced by the end of the call. The long call shares several similarities with the long calls of the sympatric species Suguinus fuscicollis nigrifrons and S. f: fuscicollis [see Hodun et al, 1981, for sound spectrograms]. The calls of both species are similar in duration, in frequency range, and in being constructed of several short syllables. However, the syllables of S. fuscicoElis ssp. are longer with fewer syllables per call, and they contain an unmodulated flat initial portion before a terminal modulation. In the field, both species responded to the long calls of the other.

For the individuals whose calls are shown in Figure 1, there were between 6 and 16 long calls available for each (X = 12.0). Although call parameters were not measured and compared, the example shown for each animal was chosen to best represent that individual. Each animal appeared to have an individually distinctive long call. For example, 18-1 had a lower fundamental frequency than the other animals. Several animals had quite different patterns in the structure of their syllables. Syllable duration and the amount of frequency modulation differed among animals. Thus, there were several variables which could be used to recognize an individual troop member on the basis of vocal cues alone.

Troop-Specific Responses to S. mystax Calls I 209

Fig. 1. Sound spectrograms of representative long calls of different animals. C-l and 18-1 are from breeding adult females; 19-2 from nonbreeding adult female; 17-1, 19-6, and 20-4 from adult males; and 20-5 from a subadult male.

The number of long calls given by separated animals and the mean latency to the first call are presented in Table II as a function of age and sex class. All animals gave about the same mean number of long calls except for nonbreeding reproductive females which gave fewer calls. Because of considerable individual variability, however, there were no statistically significant differences between groups. Non- breeding females also had the greatest latency to the first call, significantly longer

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TABLE 11. Mean Number of Long Calls and Latency to First Call

Mean No. calls Mean latency to first call (sec) Ageisex class N (-t SEMI (k SEMI

Adult male 10 10.4 (3.1) 203.2 (47.8) Breeding adult female 5 6.3 (1.9) 169.0 (49.5) Nonbreeding adult female 4 3.8 (1.6) 325.8 (66.9) Subadult male 5 6.6 (2.6) 145.9 (74.9) Subadult female 3 9.0 (3.1) 73.0 (29.6)

NON TROOP TROOP

Fig. 2. Mean percent of long calls of separated tamarins that were responded to by members of the caller’s own troop or by nontroop members.

than both subadult females (Mann Whitney U = 0, n’s = 4, 3, P < 0.03), and subadult males (U = 1, n’s = 4 ,5 , P < 0.016). No other differences were found.

Most striking was the finding that members of the separated animal’s own troop responded significantly more often to its long calls than did nontroop members. (Mean vocal response within 15 sec by troop members: 59 & 7% of separated animal’s calls; nontroop members: 4 k 1%~ of separated animal’s calls, 626) = 7.23, P < 0.001.) These results are shown in Figure 2. There were a mean of 7.83 reciprocal vocal responses per session to a separated animal’s calls by members of its own troop, but a mean of only 0.87 reciprocal responses per session were made by nontroop members. These values differ significantly from the expected values (X”1) = 11.3, P <: 0.001). These results are shown in Figure 3. Thus, the majority of observed responses to the calls of separated monkeys were from members of their own troops even though there were always more nontroop members than troop

Troop-Specific Responses to S. mystax Calls I 211

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members present during a testing session. S. mystax individuals within a troop appear to recognize and to respond selectively to members of their own troop.

DISCUSSION The moustached tamarin is similar to other tamarins tested thus far, including

the cotton-top tamarin and saddleback tamarin, in emitting a form of long call upon being separated from the rest of its troop. Nonbreeding adult females gave fewer calls than other animals and displayed a greater latency to the first long call. Subadult, animals of either sex had the shortest latency to calling. These results may reflect the relatively low status of nonreproductive mature females and the relatively greater fearfulness of younger animals on being separated.

The long-call structure of the moustached tamarin is similar to that of its sympatric tamarin species, the saddleback tamarin S. fuscicollis. In both species the calls last 2-3 sec, consist of several short, frequency-modulated syllables, and have a frequency range of 8-12 kHz. The calls are also relatively similar in structure to the closely related tamarin, S. Zabiatus (A. Hodun & C.T. Snowdon, unpublished observations). The moustached tamarin does differ from the saddleback tamarin in having shorter and more frequent syllables and in lacking the initial flat unmodu-

212 I Snowdon and Hodun

lated section crf the saddleback tamarin long-call syllable [Hodun et al, 19811. Thus there are still identifiable species differences, although there are cross-species simi- larities in long-call structure. However, all of the long calls of Amazonian tamarins differ significantly in structure from those of the tamarins found along the Carrib- bean coast. Saguinus oedipus and S. geoffioyi have long calls consisting of only 2-4 syllables, each syllable being 600-800 msec in length. In addition, the frequency range of long calls of these species is 2-3 kHz and the syllables are flat, unmodulated whistles [Cleveland & Snowdon, 19821. We can only speculate on why tamarin long- call structure differs between Amazonian and non-Amazonian tamarin species. These differences may reflect the relatively long geographical separation of the two groups of species, or they may reflect differences in habitat that make different forms of long {calls more adaptive. Only the long-call structure of the non-Amazonian species fits the characteristics described by Waser and Waser [1977] as ideal for long- distance transmission.

Although one can characterize a species-typical form of cohesive long call for the moustached tamarin, there also appear to be individual differences in the structure of the calls. These differences may provide the acoustic basis for individual recognition. Indeed, the results of the study showed that individuals are recognized, since the great majority of long calls produced by isolated individuals were re- sponded to by members of the individual’s own troop. Additionally, when all calling exchanged between animals was analyzed, the degree of reciprocal calling between the members of one troop was significantly greater than that between members of different troops. These findings, therefore, add moustached tamarins to the list of arboreal and territorial species in which indivdiual recognition can be shown to exist for all members of a social group. The existence of individual recognition for all group members implies that groups are stable enough to allow troop members to learn the individual features of each other’s calls.

CONCLUSIONS 1. The moustached tamarin Saguinus mystax gives long-call vocalizations when

separated from its group. 2. These calls are generally similar to the long calls observed in comparable

contexts in other tamarins from the Amazon, but there are species-specific fea- tures to the moustached tamarin calls. 3. Individual differences are discernible in the long-call structure. 4. The calls of separated animals were responded to primarily by members of

their own troop, implying that individuals within a troop can be recognized by voice and that troop structure is likely to be both stable and integrated.

ACKNOWLEDGMENTS This research was supported by U.S. Public Health Service grant MH 29,775,

by National Science Foundation grant BNS 78-16267, a University of Wisconsin Graduate School Research Committee Travel grant, and US. Public Health Service Research Scientist Development Award MH 00177. We thank M. Duorojeanni, C. Ponce, and R. Ruiz of the Peruvian government, and W.R. Kingston and C. Malaga of Proyecto Primates, Iquitos, Peru for their cooperation and advice. We are espe- cially grateful to Pekka Soini of Proyecto Primates for his knowledge and assistance in the field.

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