vocal exchanges between familiar cotton-top tamarins

The Japanese Journal of Animal Psychology, 50, 1, 95-102 (2000)

Original Article

Vocal exchanges between familiar cotton-top tamarins

during social isolation

YOICHI KURETA1 2 3

Primate Research Institute, Kyoto University, Inuyama-shi, Kanrin, 484

Abstract Captive cotton-top tamarins produce variant forms of "long call" when separated from their social companions. In this article, vocal exchanges between familiar cotton-top tamarins during visual isolation were investigated experimentally. Two randomly selected subjects were separated from their colony, and were visually isolated into the separate cages in the same testing room. Antiphonal long calls within the restricted time period were more frequently observed between cage-paired tamarins than expected by chance. From this experimental finding, functional significances of the long calls during social isolation were discussed in conjunction with the previous findings in other primates of the New World, including tamarin and marmoset species. Key words cotton-top tamarins, long call, vocal exchange, familiarity, social isolation.

Callitrichidae, the tamarin and marmoset family is noted for pair-bond formation (e. g., Epple, 1975). This social organization is likely to be formed and maintained by means of species-specific communicative interactions not only within a family group but also between groups. For example, the male common marmoset, Callithrix jacchus, puts in/out its own tongue on approaching the paired female before

copulation, but turns the caudal part of the body

and shows the genital toward intruders

(Stevenson & Poole, 1976). In addition to visually distinctive display, acoustic communication is an

important adaptation for forest-dwelling

primates, and plays a central role in maintenance of their social relations (Waser, 1977). In aid of vocal signals, the callers are able to keep contact

with familiar animals within the same group,

while keeping unfamiliar animals outside the

group far apart (Robinson, 1979; Robinson, 1981). Within callitrichid vocal repertoires, the "long

call" has been considered as the most

conspicuous and species-specific vocalization for

organizing social relationships. The first true

investigation dates back to Moynihan's (1970)

field research in which three functions were

suggested as follows: (1) territorial defense

against conspecifc intruders; (2) intra-group

cohesion and mate attraction; (3) locating

separated animals during traveling and foraging

through the forest. In past decades, the usages of

long calls have been examined and found to be

in agreement across many callitrichid species

(see Snowdon, 1989). In the laboratory, cotton-top tamarins,

Saguinus oedipus, have been extensively

1 Reprint request e-mail : kureta@ tmig. or. jp 2 Present address : Tokyo Metropolitan Institute

of Gerontology, 35-2 Sakae-cho, Itabashi-ku, Tokyo 173-0015, Japan (Tel: 81-3-3964-32419)

3 The author thanks Prof. S. Kojima, Prof. N. Masataka and Dr. H. Sugiura for their valuable advice and encouragement, and also S. Nagumo for his help in technical assistance of instrumentation. The author is grateful to Miss N. Matsubayashi for her help in daily care of animals, and to the staffs of the Department of Phylogenetic and Systematics in the Primate Research Institute for their permission to use their computer and printer, and to Dr. Robert Mintzer for his correction of writing. Finally, the author would like to thank two reviewers for helpful comments and discussions. This study was supported by a Grant-in-Aid for Scientific Research # 3111 from the Ministry of Education, Science and Culture, Japan.

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The Japanese Journal of Animal Psychology, 50, 1

investigated with regard to long call behaviors accompanied by complex social interactions

(Cleveland & Snowdon, 1982; Snowdon, Cleveland, & French, 1983; McConnel & Snowdon, 1986), whereas comparable

examinations which focused on free-ranging cotton-top tamarins were limited to one earlier field research (Neyman, 1977). Cleveland & Snowdon (1982) initially documented that captive cotton-top tamarins possess and differentially use a wide variety of vocal repertoires representing distinctive communicative messages. The authors found that long calls can be divided into three acoustic variants, each of

which is associated with three separate contexts as described above (Moynihan, 1970). A subsequent study based on the playback

paradigm demonstrated that cotton-top tamarins are capable of discriminating between vocally familiar versus unfamiliar calls, because the subjects showed stronger responses only toward calls emitted by animals outside their own group (Snowdon et al., 1983). Furthermore, antiphonal responses, which the previous study failed to show by means of the playback

paradigm, were significantly evoked when inter-group encounters were simulated by

exposing the tamarins to naturally-occurring long calls from less familiar tamarins housed in other colony rooms (McConnel & Snowdon, 1986).

While Snowdon and his colleagues have shed light on the contextually specific uses of two types of long calls emitted by cotton-top tamarins, little is known about the third

presumable function during brief isolation from a subject's own group members. In the early field observation, separated cotton-top tamarins exchanged long calls with one another, approaching toward the source of the calls

(Neyman, 1977). Similarly, Moynihan (1970) documented that Saguinus geoffroyi, a species

closely related to cotton-top tamarins (no English vernacular name), used long calls as "lost calls" during separation. Insofar as tamarins were separated from one another, it is reasonable that long calls are sent toward familiar individuals within their own group rather than unfamiliar ones outside the group. In the case of the moustached tamarin (Saguinus mystax), group

members were more likely to respond to long calls emitted by isolated individuals, and reciprocal calling also occurred more frequently

between group members than between non-group members (Snowdon & Hodun, 1985). This finding may be taken as evidence that long calls are given to familiar rather than unfamiliar individuals while they are socially separated.

The study reported here was designed to find evidence for such biased use of long call exchanges between familiar cotton-top tamarins

during a brief visual separation experimentally imposed on them, beyond the descriptive findings reported so far (e. g., Neyman, 1977;

Cleveland & Snowdon, 1982). The experimental methodology was to separate two randomly selected subjects from their own home cages, and to allow them to exchange long calls ad lib without visual information. As hypothesized

above, if long calls function to keep contact within group members during social separation,

communicative interactions based on the calls should be more often between familiar cage mates than between unfamiliar non-cage mates.

Method

Subjects and housing condition

The subjects were six adult cotton-top tamarins (Saguinus oedipus oedipus) born in captivity, including two males and four females

(Table 1). Although this species is currently an endangered species, ancestors of our colony had been legally housed in the Primate Research Institute of Kyoto University.

Table 1. Subjects and housing condition.

96

Kureta : Vocal exchanges between familiar cotton-top tamarins during social isolation

At the beginning of the present experiment,

the colony consisted of 25 cotton-top tamarins.

Animals were kept separate within the same

room in wire-meshed cages measuring

approximately 50 X 50 X 100 cm, in which wooden

branches, ropes and a nest box were equipped for

their daily use. The population of each cage

varied from two to six individuals. The home

cages were arranged so that neighboring animals

could not make visual contact with one another

but vocal and olfactory communication was

possible.

The subjects had been paired in their home

cages for three years or more prior to the

beginning of the experiment; one of these pairs

was a female-female pair and the remaining two

were male-female pairs (Table 1). Both of the

male-female pairs had offspring who were

separately housed in other cages within the same

room at the beginning of the experiment. The

subjects SO40 and SO50 had been housed

together for more than 10 years. Of the

female-female pair, SO57 had also produced

offspring who were not present in the colony

room, but SO142 had not. Although subjects

SO40, SO50 and SO57 were extraordinarily old,

they were used because of sufficient long-call

productions during visual separation.

All animals were fed daily with SPS marmoset

diet (CLEA Japan) plus pieces of fruits, and

occasionally with powdered milk, sweet potatoes

and mealworms. Room temperature was always

controlled by air-conditioner to 20-25•Ž

regardless of seasonal fluctuations outside the

room.

Apparatus

For the purpose of isolation, two test cages

made of steel grids (45 •~ 45 •~ 65 cm) were prepared

in a sound-attenuated room (4 •~ 2 •~ 2.5 m). The

cages had two horizontal wooden perches 3 cm

in diameter, and were separated 1.5 m away from

each other by a 45 •~ 80 cm wooden board which

restricted visual contact but allowed auditory

and olfactory communication between subjects.

Vocal behaviors were recorded using a digital

audio recorder (Sony TCD-10) and two

directional microphones (Audiotechnica AT-

815b) placed in front of the cages. Simultaneous

data collection from two individuals could be made using double-recording tracks of the tape

recorder.

Procedure

Two subjects were individually transported and isolated in each of the test cages in the

presence of a white noise masking (80dB SPL). One subject was first confined into the cage on one (right) side, followed by taking the other subject into the other cage on the opposite (left) side after 5 min. This sequence, which was maintained throughout the experiments,

prohibited visual contacts between the subjects during transportation. As soon as the white noise masking was extinguished, recordings were taken of calls occurring during a 15 min period

per session. I constructed a combination matrix of

subjects (left x right), and randomly selected one cell per testing day until all cells composed of the 30 possible pairs were completed, with caution taken so that a given combination did not occur consecutively. At the end of testing, each subject was experimentally paired with all possible other subjects twice. To prevent habituation, the same subject was never repeatedly tested within a week. In preliminary observations prior to the

present study, all subjects were confirmed to produce sufficient long calls (10 calls / 15 min) when completely isolated from their partners.

Figure 1 shows typical sound spectrograms of long calls produced by each subject during isolation. The structure can be broadly divided into two components: introductory chirp(s) and the subsequent whistles. The whistle unit is the representative structure defined as a "long call." The combinational form appeared to fit the

previous description of "combination long call" or possibly "type F chirp + whistle" (Cleveland & Snowdon, 1982). The authors initially reported that combination long calls act as "lost calls" when produced by separated animals

(Cleveland & Snowdon, 1982), whereas such calls have been regarded as an immature form exclusively used by non-reproductive animals in subsequent reports (Snowdon et al., 1983; McConnel & Snowdon, 1986). However, the sexually mature subjects reported here

97


sufficiently produced the combination type of long calls when visually separated. Furthermore, since the definition of the variant forms was not straightforward, long calls were not divided into subtypes in my data collection insofar as they had whistle syllables. In addition to this type of

long call, the subjects independently produced several types of chirp signals, which were not followed by whistle syllables. However, in the

present study, vocal exchange was considered in terms of a sequence between consecutive long calls, which were most frequently heard during isolation.

Data analysis

Previous studies of other species

(Masataka & Biben, 1987; Sugiura, 1993) showed that vocal exchange is regulated by the temporal

rule, resulting in representative distribution of

intervals between two consecutive calls. To

determine whether consecutive calls are

independently emitted or evoked by a preceding

caller in cotton-top tamarins, the distribution of

inter-call intervals (ICI) was constructed. This

analysis was expected to extract vocal responses

to the preceding call for further analysis.

The call data were analyzed using a

computer-based sound spectrogram (KAY model

CSL50), together with a real-time counter (built

in the tape recorder) accurate to 1 sec. ICI was

defined as the duration from the end of the

preceding call to the beginning of the next call

(Figure 2). I measured all intervals inserted between long calls occurring during a 15 min

session. The ICIs were measured by placing a

calibrated grid on the spectrogram for intervals

shorter than 10 sec, whereas the real-time counter

was used in the case of ICIs longer than 10 sec.

After 30 pairing test sessions (450 min total)

were complete, a matrix of observed frequencies

was reconstructed to a caller x recipient matrix,

and compared with expected frequencies using

a chi-square test for significant deviations. In the

experimental design in the present study, the

matrix always had empty cells in the major

diagonal, because the same animals did not serve

as caller and recipient in the same vocal

sequence. Expected frequencies of the diagonal

cells were then estimated using an iterative

procedure called the Newton-Raphson algorithm

(Bakeman & Gottman, 1997; Finberg, 1980). To

Figure 1. Representative sound spectrograms given by six subjects.

Figure 2. Definition of inter-call interval (ICI).

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identify probabilities deviating from expected

values (normal distribution), adjusted residuals

(equivalent to Z-score) were also calculated from the log-linear model program. If the score in each cell is larger than 1.96, it is statistically significant

(p < .05).

Results

Of 831 long calls recorded, 801 sequences of long calls occurred during a total of 30 sessions. Two ICI histograms were constructed with respect to the participants in the sequences, as shown in Figure 3. The distribution of ICIs

between different callers (N =466) showed a

pattern having a representative peak between -1 and 2 sec following the preceding call (37.1 %). The corresponding peak was lacking in the ICI distribution between the same callers (N =335), indicating that the same individuals did not repeat long calls within 2 sec. Then, assuming the

second calls given in the interval from -1 to 2 sec

as responses to the preceding calls, sequential analysis was performed to examine whether significant deviation might exist in vocal exchanges between particular individuals.

Table 2 shows a transition matrix (preceding

callers in rows X subsequent callers in columns) of the observed frequencies (expected frequency in parentheses) among six subjects (chi-square= 31.9, df =19, p < .05). As mentioned earlier, I assumed that the observed frequencies were distributed normally, with adjusted residuals larger than 1.96 absolute regarded as statistically

significant. The scores computed using the log-linear model algorithm are shown in Table 3. SO50 was significantly responsive to the calls

given by SO40, who had been paired with the recipient in a home cage. Similarly, SO142 significantly uttered long calls in response to the

preceding calls by its cage-paired subject, SO57. SO135 was also most likely to respond toward the cage-paired subject, SO125, than expected by

chance.

The results of sequential analysis failed to show a reciprocal relation of a caller-recipient

sequence between any pairs. However, there was a likelihood for subjects SO40, SO57, and SO125 to respond toward calls given by their cage mates. For example, SO40 responded toward the calls

Figure 3. Distributions of ICI by the different callers (upper) and the same callers (lower).

Table 2. Observed (expected in parenthesis) frequencies for vocal sequences between two isolated tamarins within the restricted period from -1 to 2sec.

Table 3. Adjusted residuals for Table 2.

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given by SO50 more than to those by other subjects. Relatively, both SO57 and SO125 were also likely to respond toward calls given by their cage-paired subjects, SO142 and SO135, respectively. Thus, vocal responses were likely to

be toward cage-paired subjects, although the values did not significantly differ from what was expected by chance.

On the other hand, analysis of second calls outside the intervals from -1 to 2 sec could not well account for the cohesive relation derived from the familiarity of home cages (Tables 4 and

5). Chi-square test showed that distribution significantly deviated from that expected by chance (chi-square= 38.8, df =19, p <.01). Significantly negative deviation, for example, between the sender SO57 and the recipient SO125 may be due to the fact that in the experimental session, there was an increase in call sequences

between the same callers, whereas there was a decrease in call sequences between different callers. In this context, one subject tended to repeat long calls while the other was silent for the time being. As a result, alternation of calling was rare even outside the interval from -1 to 2 sec. Similar phenomena could be observed in the other case of non-cage mates, but not among cage mates.

These results, taken together, suggest that

cotton-top tamarins tend to exchange long calls more often between familiar individuals following a limited time rule.

Discussion

The results reported here illustrate familiarity effects on the likelihood of vocal exchanges among six captive cotton-top

tamarins. The factor of whether a home cage has been shared or not in a daily housing condition can be a critical determinant for the subjects to regulate vocal responses while they are visually separated from each other. Vocal responses are more prone to be evoked within a rigorous time window between -1 and 2 sec following long calls emitted by a cage mate. The tendency appears to

be consistent with that reported for the moustached tamarins, where vocal responses were significantly more often within a 15 sec

period by their own group members than by non-group members (Snowdon & Hodun, 1985), although the temporal windows specified as a criterion of vocal exchange differed between the two studies.

The cotton-top tamarins in the present study were always located in the immediate vicinity of each other, 1.5 m apart. The experimental context employed here seems to be somewhat limited in light of the mimicry of naturally-occurring social

separation, given that foraging cotton-top tamarins might spread out up to 35 m or more in the wild (Neyman, 1977). There is no reason, however, to suspect that the vocal exchange occurs exclusively at such long distances. Field observations have reported that production of long calls by a separated tamarin usually continues to, and stops immediately after

rejoining with the group members in sight

(Moynihan, 1970; Neyman, 1977). Such a reaction, combined with the dense vegetation constraining visual contact in callitrichid habitats, suggests

that tamarins produce long calls even at close distances, insofar as visual information of their

group members is not available. However, a minor modification of specific call parameters might be shown compared to those of long calls

given at long distances. In other species of the New World primates, squirrel monkeys, Saimiri

Table 4. Observed (expected in parenthesis) frequencies for vocal sequences between two isolated tamarins outside the restricted period from -1 to 2sec .

Table 5. Adjusted residuals for Table 4.

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sciureus, modify the structure of contact calls as

a function of the distance between individuals

allowing for efficient sound localization

(Masataka & Symmes, 1986; see also Snowdon &

Hodun, 1982).

As demonstrated in the present study, other

species have been reported to use antiphonal

calling at short distance between particular

individuals. Snowdon & Cleveland (1984), for

example, have demonstrated that pygmy

marmosets, Cebuella pygmaea, exchange calls in

rapid sequence among particular individuals

more often than expected by chance within an

enclosure measuring 4 •~ 4 •~ 3 m. The authors

discussed that in wild populations, such a vocal

sequence enables pygmy marmosets to forage

while keeping close contact within a group out of

sight. Similarly, Masataka & Biben (1987) have

reported that in a spatially limited enclosure (3.0

m high x 3.6 m diameter size), squirrel monkeys

are likely to produce contact calls as a function

of affiliative interactions. However, caution is

urged when comparing the previous studies to

the study reported here, because it remains

unclear whether the variant of cotton-top tamarin

long calls induced by visual separation can be

functionally isomorphic to the contact calls

spontaneously given by the other species of

primates noted above. Furthermore, it is

suspected that transporting and confining the

subjects to small test cages has inevitably caused

a state of distress in my experimental procedure.

I failed to find statistical significance of

reciprocal calling in any pairs. One possible

explanation is that the roles of caller and

recipient are separated between individuals

according to some physical and/or social

attributes. It has been suggested that the usage

of long calls should be considered in terms of sex,

age and reproductive status (e. g., McConnel &

Snowdon, 1986; Snowdon, 1989). In the cotton-top

tamarin, mature females of pair-bonded adults

produce territorial long calls more often than any

other group members (McConnel & Snowdon,

1986). It is reasonable to think that the roles of

sender and recipient may differ between sexes,

because all three subjects who significantly

served as a sender in the present study were

females. However, the sex difference may not be

so rigid in the context of a brief social isolation,

given that occasions to separate during foraging are not necessarily restricted to mature females among the group. This notion appears to be congruent with the present finding in that vocal exchanges could be significantly observed beyond male-female pairs, as shown by contact calls of pygmy marmosets (Snowdon &

Cleveland, 1984). As far as the two extraordinarily long-lived

subjects, SO40 and SO50, were concerned, exchanges of long calls seemed to be more reciprocal than in the other pairs. Despite no statistical significance in one direction (adjusted residual: 1.44), their score is considerably high relative to those of the other pairs (adjusted

residual: 0.66 and 0.77, respectively). Notably, the old subjects have been housed together for more than 10 years. This finding suggests that how long tamarins have been exposed to one another could be an alternative index of degree of familiarity. Due to the small number of subjects used in the present study, further explorations are needed to clarify the mechanism of long call

behavior during social isolation.

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(Received Oct. 4, 1999 ; accepted April 18, 2000)

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