- Email: [email protected]
Temporal and structural features of infant calls in relation to caregiving behaviour in common marmosets, Callithrix j. jacchus
BEHAVI~~~~ PROCESSES ELSEVIER
Behavioural Processes 38 (I 996) 183- 19I
Temporal and structural features of infant calls in relation to caregiving behaviour in common marmosets, Callithrix j. jacchus’ Stefan Geiss, Lars Schrader Institutfir
Verhaltensbinlogiu,
*
FU Berlin, Haderslebener Strabe 9, D-12163 Berlin, Germany Accepted 2 April 1996
Abstract The role of infants in the communal rearing system of marmosets and tamarins has received little attention although their demands may not be complied by inadequate helpers. As acoustic signalling plays an important role in their social communication, it is expected to be an effective way for infants to signal their demand for care. As a first approach, this study focussed on the use and quality of ‘tsik’ calls given by infants of common marmosets (Cullirhrix j. jucchus) in the context of caregiving. The acoustic and non-acoustic behaviour of a group of common marmosets were recorded during the first two weeks of the life of two infants (twins). Vocalizations were classified, and the structure of the infants’ ‘tsik’ calls was quantified by measuring specific signal parameters. Infants gave ‘tsik’ calls in close temporal relation to caregiving behaviour. Specific parameters covaried with the subsequent behaviour of potential caretakers. Values of call duration, start frequency, peak frequency, and range were lower when infants’ calls were followed by no reaction or an approach of group members, whereas these parameters showed higher values when followed by a transfer of infants. Our results suggest that the actual demand of infants is encoded in the variations of ‘tsik’ calls. Keywords:
Acoustic parameter;
Caregiving
behaviour;
Common marmoset;
Communal rearing system; Vocalization
1. Introduction In the communal
rearing
system
of marmosets
and tamarins
(Callitrichidae)
only
the dominant
female reproduces, but all other group members are involved in carrying and taking care of the infants (Goldizen, 1990; Stevenson and Rylands, 1986; Sussman and Garber, 1987). The advantages to the mother resulting from this social system are quite obvious. Usually she gives birth to twins, the
* Corresponding author. ’ Based on a contribution to the Bioacoustics and Man’ (Merbitz, Germany, 1995).
Workshop
0376.6357/96/$15.00 Copyright 0 1996 Elsevier Science P/I SO376-6357(96)00022-S
‘Numerical Methods for the Study of Vocalization
B.V. All
rights reserved.
in Animals
weight of which is almost 20% of the mothers weight. Carrying the infants impairs foraging in a period of time when her metabolism is greatly accelerated by demands of lactation (Tardif, 1994; Terborgh and Goldizen, 1985). Adult males are the primary infant carriers, and the extent of infant-care of other group members, mostly siblings of the newborns, increases with age (Ingram. 1977; Tardif et al., 1992; Terborgh and Goldizen, 1985). Although often more than one adult male may be reproductively active, adult males may profit directly in rearing their potential offsprings (Terborgh and Goldizen, 1985), and they may influence future female mate choice in demonstrating their skills in infant care (Ferrari, 1992; Price, 1991). The other group members can profit by enhancing their inclusive fitness by kin selection, acquiring experience in parental behaviour. developing cooperative relationships or increasing their chance of inheriting the territory later on (Emlen, 1991; McGrew and McLuckie, 1986; Price, 1991; Terborgh and Goldizen, 1985). Most of the studies on the communal rearing system in marmosets and tamarins have focussed on the caregivers, whereas the role of infants has received little attention. However, the need of infants is a crucial factor in the evolution of this social system and should be reflected in the social interactions between infants and caregivers. One main interest of infants is to obtain enough milk from their mother. Hence, it is crucial for them to be transferred to their mother whenever they need food. If their mother does not take the infants by herself in regular intervals, the infants should be able to signal their demand. As infants are quite dependent and immobile they should be interested in receiving care from experienced group members. Handling by young and unexperienced group members may pose potential risks of inadequate care for the infants (Engel. 1985; Price, 199 1; Riechelmann et al., 1994). Competition between group members to carry infants may also impair the quality of care. Furthermore, adults may intervene attempts of younger group members to retrieve infants (Price, 1991). Hence the lower proportion of young group members that help in infant care may reflect the attempt of experienced adults to reduce the risk of inadequate care. Thus. again, infants should be able to signal that they are treated inadequately. Acoustic signalling plays an important role in communication between and within groups of marmosets and tamarins (Boinski. 1991; Caine and Stevens, 1990; Schrader and Todt, 1993; Snowdon et al., 1983; Snowdon and Cleveland, 1984). Due to the dense vegetation of South American rain forests, visual contact is often restricted. According to these constraints on communication facial expressions in New World monkeys are not well developed compared to those in Old World monkeys (Andrew, 1963). Hence, acoustic signalling is expected to be a more effective way for infants to signal their demand to potential caregivers. The aim of this study was to investigate the role of acoustic signalling in caregiving. We focussed on vocalizations of infants to investigate whether and how the behaviour of group members covaries with infants’ signalling behaviour. Such covariations would indicate that infants are able to signal their demand acoustically. We focussed on the following specific questions: (a) do infants of common marmosets use specific vocal patterns in the context of caretaking?; (b) are there temporal correlations between specific infant vocalizations and the behaviour of caregivers?; and (c> how do characteristics of infants’ calls covariate with specific behaviours of caregivers? 2. Materials and methods We studied a family group of 9 common marmosets ( Callithrix j. jacchus) ( 1 adult female, 2 adult males, 2 sub-adult males, 2 juvenile males, 2 infants) housed together in an indoor wire meshed cage
S. Griss.
L. S~,hrud~r/Behal,iourcrl
Pmcessr.~
38 IIYY6I
183-191
185
(3.5 X 2.5 X 2 m) enriched with branches and nest boxes. In order to optimize acoustic conditions, room walls were covered with unechoic material. Subjects were observed daily during the first two weeks after the birth of the youngest infants. Observation sessions were distributed randomly over the activity phase of the group, and on each day 2 to 4 observation sessions were conducted. A total of 30 h were recorded, including 78 transfers of infants from one group member to another one. Social interactions (approaching , grooming, grasping, olfactory control, tugging and transfer) shown by group members directed to infants as well as suckling were recorded continuously with a mini computer (Atari portfolio; software: BEHAVIOR 2.3, developed by Kurt Hammerschmidt and Lars Schrader). Vocalizations were recorded with a tape recorder (REVOX PR 99, 7.5 cm/s; Sennheiser ME 80). Whenever we saw that a given subject, and especially an infant, was vocalizing, this was commented on the second channel of tape recorder. We used 3 subsets of the total sample to analyse vocalizations. As our criteria to select these subsamples depended on the respective step of analysis, they are explained in the results. Vocalizations were classified by visual inspection of spectrograms, following the definition by Winter and Rothe (1979) and using software for real-time spectrograms CRTS, Engineering Design, Boston, MA, USA). As a result of an initial analysis of vocal patterns, we focussed on the ‘tsik’ calls given by the infants. As vocal patterns of infants were highly variable (cf., Winter, 1977) only calls with an up-sweep from start frequency to peak frequency followed by a down-sweep to end-frequency were defined as ‘tsik’ calls. Intermediate forms of ‘tsik’ calls with other call types were not considered. Due to their different pitch, infants’ ‘ tsik’ calls could be distinguished unambiguously from ‘tsik’ calls of other subjects. Parameters of ‘tsik’ calls were measured using RTS (frequency range: 16 kHz, frequency resolution: 79 Hz, time resolution: 7 ms). We quantified the structure of ‘tsik’ calls by using the following parameters (see also Fig. 1): (1) start frequency, (2) peak frequency, (3) end frequency, (4) duration, (5) frequency range (i.e., peak frequency-end frequency), (6) frequency increase (i.e., peak frequency-start frequency), (7) frequency decrease (i.e., peak frequency-end frequency), (8) time-structure (i.e., duration of frequency increase/duration of frequency decrease), (9) frequency-structure (i.e., frequency increase/frequency decrease), ( 10) frequency decrease per time (i.e., frequency decrease/duration of frequency decrease). We used SPSS for Windows 6.0 for statistical analysis. Univariate covariations between rearing contexts and acoustic parameters were tested with a Kruskal-Wallis one-way ANOVA. Discriminant
1
2
3 Time [s]
Fig. 1. Spectrogram of a series of five ‘tsik’ calls given by an infant of common marmosets. Signal parameters measured in spectrograms were (a) start frequency, (b) peak frequency, (c) end frequency, and (d) duration.
analysis was applied to check whether vocalizations could be distinguished statistically between sub-contexts (defined below). The discriminant analysis compares multivariate patterns resulting from any interaction of variables. It provides a classification procedure that assigns each call either to its appropriate group (correct assignment) or to another group (incorrect assignment). Furthermore, it calculates a rank order in which parameters are important for distinguishing among groups.
3. Results All group members took part in carrying the infants during their first two weeks of life. In total, the mother carried one or both infants in 19% of cases, the dominant male in 39%, the other adult male in 17%, the two sub-adults in 23%, and the two juveniles in 3% of all observed instances. To calculate an overall budget for vocalizations we randomly selected a sample of 1 h from our observation time of 30 h (sample (I)). We excluded phases in which high vocal activity were most likely caused by external stimuli (e.g., sudden appearance of a bird in front of the window) and phases with no activity (e.g., the whole group was resting) from analysis. This sample (I) included 2500 vocalizations. Within sample (I) 68% of calls could be classified as ‘phee’ calls, 12% as ‘tsik’ calls, 10% as ‘qua+ calls, 7% as ‘twitter’ calls, and 3% as other call types (cf., Winter and Rothe, 1979). 93% of the ‘tsik’ calls in this sample were uttered by the two infants. In the next step of analysis we focussed on the interactions between group members and infants. These interactions included approaches of group members to the infants as well as transfers. As a result of the preceding analysis, we only included interactions during which ‘tsik’ calls were given by infants. This sample (11) again was selected randomly from the overall observation of 30 h. In total, 6 h were covered, and 2310 ‘tsik’ calls of infants and 28 transfers were included. 58% of the infants’ ‘tsik’ calls were given within 2 min before infants were transferred. The remaining 42% of ‘tsik’ calls were most often also followed by a reaction of group members (e.g., approach), but were not followed by a transfer. When ‘tsik’ calls were given by infants without a following transfer call rate of infant ‘tsik’ calls was 3.1 calls per min. In contrast, call rate increased to 26.4 calls per min in the time window of 2 min before a transfer took place. In a third step we analyzed the relation between infant ‘tsik’ calls and the succeeding behaviour of group members in more detail. Within 2 min after the onset of infant ‘tsik’ calls we defined four behavioural contexts, based on the behaviour of group members: (A) a group member approached but did not take the infant; (B) a group member approached and took the infant; (Cl a group member immediately took the infant as contact had already been established; (X) ‘tsik’ calls were not followed by any reaction of group members within these 2 min. This sample (III) was identical to sample (II), but in order to test for covariations between call structure and behavioural contexts, we selected 633 ‘tsik’ calls from the total of 2310 to measure signal parameters. All call parameters measured, except the frequency decrease per time, covaried significantly with the different behavioural contexts (Kruskal-Wallis H test, P < 0.001). Fig. 2 shows an example of four parameters. The values of start frequency, peak frequency, frequency range and duration increased from context (X) over context (A) to context (B), whereas the values in context (C) were at least lower than in context (B). The discriminant analyses showed that the acoustic structure of calls from the 4 sub-contexts clearly differed. 58% of calls were correctly classified (random assignment 25%) (Table 1). Best
187
Start
Frequency
Peak Frequency
12
l3 1
11
*
2 y 10 z
t
Y
a)
I
8
A
+ +
*
7’X
t
%ll 5 3 z z lo-
5 z 9
E
.
p 12 -
B
C
b)s-
X
A
8
C
Subcontext
Frequency
Range
Call Duration
t
+
t t cl
3'X
A
B
C
cl)
so
Subcontext
X
A 6 Subcontext
C
Fig. 2. Means and standard error of the (a> start frequency, (b) peak frequency, (c) frequency range, and (d) call dLIration of ‘tsik’ calls given by infants. Sub-contexts were defined due to the behavioural reaction of group members after onset of infant calting: (X> no reaction (n = 1401, (A) approach (n = 1401, (B) approach and transfer (n = 331), and (C) immediate transfer (11= 22).
predictor variables were (I) start frequency, (2) peak frequency, (3) frequency range, and (4) duration (Fig. 2). When contexts were combined in a context ‘transfer’ (context B -t context C) and a second context ‘no transfer’ (context A + context X), 92% of calls were classified correctly (random assignment 50%) (Table 1).
Table 1 Result of discriminant
anal-&+
Actual sub-context
X: A: B: C:
No reaction Approach Approach with transfer Transfer
Predicted membership
to sub-context
X: No reaction
A: Approach
B: Approach with transfer
C: Transfer
n
64% (89) 34% (48) 2% (6) 0% (0)
30% (42) 56% (79) 7% (22) 0% (0)
4% (6) 6% (8) 54% (179) 18% (4)
2% (3) 4% (5) 38% (124) 82% (18)
140 140 331 22
Infants’ ‘tsik’ calls were classified in the four sub-contexts on the basis of measured signal parameters. assignment and the total number of assigned calls (in parentheses) is shown.
The percentages
of
188
4. IXscussion Our results provide the first evidence that the ‘tsik’ calls of common marmoset infants may contain information about their actual demand for care. The performance of infants’ ‘t&k calls was associated with social interactions between group members and infants. In particular, we found temporal relations between the onset of the infants ’ ‘tsik’ calls and the succeeding behaviour of group members. Within 2 min after the infants started calling, most often a group member approached or took the infant. Moreover, the type of reaction (no reaction, approach, approach and transfer, immediate transfer) covaried with certain structural features of the infants’ ‘tsik’ calls. Although our sample size is still relatively small, the results suggest that infants have the potential to play an active role in caregiving behaviour. Our data on the percentage of time the different group members carried the infants are in line with observations of other studies on captive common marmosets. In the first two weeks the infants were carried mainly by their mother and the adult males, less by the two sub-adults and the two juveniles (cf., Box, 1977; Engel, 198.5; Ingram, 1977). This indicates that caregiving behaviour of the group we studied was similar to that in other groups of captive common marmosets. ‘Tsik’ calls were given predominantly by infants and in close temporal relation to caregiving behaviour. The use of specific vocal patterns by infants in relation to caregiving is well known in humans and in nonhuman primates. In human babies as well as in infants of Old World monkeys these vocal patterns most often consist of cry series (for reviews, see Todt, 1988, 1996). Cries are complex vocal patterns, characterized by large frequency ranges, noisy and shrill frequency features, and a high variability of acoustic parameters within a series of crying. In contrast, ‘tsik’ calls of common marmosets have a rather simple acoustic tonal structure. However, common marmosets also produce another call type, the squeal call or ‘qu%-r’ call (Winter and Rothe, 19791, which has similar signal characteristics as the cries of human babies and of nonhuman primates’ infants. In common marmosets there are only a few studies about the use of vocalizations of infants or about vocal ontogeny (cf., Newman, 1995). Winter (1977) described infant vocalizations on the day after birth and found four call types which were very variable in structure and were uttered in no constant sequence. In addition, intermediate patterns of call types occurred regularly. Call types could not be related to specific situations. Instead, they seemed to indicate unspecific distress. Also Epple (1968) noted that, with increasing distress, infants give series of ‘tsik’ call, twitters and squeals. Our observations suggest that the squeals were given predominantly by the two juvenile males during their mostly unsuccessful and dismissed attempts to take the infants from older group members. Infants gave ‘tsik’ calls much more often than other group members, although call sequences could include not only ‘tsik’ calls but also other vocal patterns. Adult common marmosets give ‘tsik’ calls in aversive situations, for example when mobbing a predator (Epple, 19681, if unfamiliar persons approach their cage, or when subjects are caught for physical examination (personal observations). Hence, ‘tsik’ calls might indicate a senders’ discomfort or distress. Our results indicate that with the quality of infants’ ‘ tsik’ calls the behaviour of possible caregivers covaried. Lower values of call duration, start frequency, peak frequency, and range in the infants’ ‘tsik’ calls were followed by no reaction or an approach of group members, while ‘tsik’ calls with higher values of these parameters were followed by a transfer of infants. Discriminant analyses showed that due to their structure these v~iations of infants’ ‘tsik’ calls could be assigned clearly to the type of behaviour that was shown by group members following the onset of infants’ calling.
Since the investigation by Green ( 1975) on vocalizations of Japanese monkeys ( Macacu f~scata), an increasing number of studies have shown that even subtle variations of a given call type may covary with social context and thus may reflect the internal state of sender. Information about the quality and the level of internal state can be deduced from temporal changes of specific par~eters (Todt, 1996; Todt and Hultsch, 1996, see also Hultsch and Todt, 1996). Nowadays computer-aided analysis of acoustic signals allows for exact quantification of such variation of vocalizations (Schrader and Hammerschmidt, in press). For the ‘phee’ call of common marmosets it could be shown in separation experiments that call duration, frequency. frequency range and amplitude increased with decreasing sensory information about mates (Schrader and Todt, 1993). Furthermore, the frequency as well as the call duration changed with increasing time of separation (Newman and Goedeking. 1992). The authors suggested that these changes may reflect the changing arousal of the sender. In cotton-top tamarins (Saguirtus oedipus) the instability of fundamental frequency was found to correlate with playful interactions (Goedeking and Immelmann, 1986). In vocalizations of squirrel monkeys (Suivniri sciureus), Jiirgens (1979) found a positive correlation between aversiveness of calls and the total frequency range in non-harmonic, noisy calls. In high-pitched harmonic calls he found correlations with the pitch of fundamental frequency and irregularity of frequency course. For Old World monkeys, covariations between frequency and frequency range and the quality of aggressive interactions were found in the screams of pigtail macaques (~ffc~~~ ~?e~~~~~~~z~) (Gouzoules and Gouzoules, 1990). In the disturbance calls of barbary macaques ( Mucaca s~lucrnus) time as well as frequency characteristics within call series shifted gradually (Fischer et al., 19951, indicating a change of internal state. in summary, the findings described above are in line with the motivation-structural rules by Morton (1977) who hypothesized a general relationship between physical structures of sounds and the motivation underlying their use. Regarding his model the ‘tsik’ calls of common marmosets might indicate a high level of fear or submission, combined with an increasing hostility. Thus. the acoustic quality of infants’ ‘tsik’ calls might reflect the arousal or emotional state which presumably is affected by the quality of care they receive. Hence infants might be able to signal their demand for a change in care. The possibility that receivers of such signals are able to distinguish subtle variations in signal structure could be shown for common marmosets (Norcross et al., 19941, cotton-top tamarins (Bauers and Snowdon, 19901, and pygmy marmosets (C&rella pq‘gmeae) (Snowdon and Cleveland, 1980; Snowdon and Pola, 1978). That vocalizations may reliably signal the need of offsprings was demonstrated with a matheInatical model by Godfray ( 1991). Hammerschmidt et al. ( 1994a,b) investigated the dusk calling in barbary macaques. At dusk, juveniles often utter heterotype series of vocalizations that last until the callers have formed sleeping clusters with other individuals. Here, too, the vocalizations might indicate their social demand. Weary and Fraser ( 1995) found in domestic pigs (Sus SCK$ ~~u~esri~a) that vocalizations of piglets in poor condition of nutrition had higher call duration and frequency parameters than piglets in good condition. They concluded that the piglets’ need was encoded in these acoustic features. Taking the findings of other studies into account, our results in common marmosets suggest that the actual demand for care is potentially encoded in variations of infants’ ‘tsik’ calls. Although the data were gathered from only one family group, our study indicates that infants may play an active role in the communal rearing system of marmosets and tamarins. Further studies may focus on signalling in dependence of the individual identity of different caregivers.
190
S. Geiss. L. Schmder/Behnc,iourul
Processrs 38 (1996) 183-191
Acknowledgements We would like to thank Jiirg Bijhner, Julia Fischer, Kurt Hammerschmidt, Marc Naguib, Cord Riechelmann and Dietmar Todt for stimulating discussions and critical comments on earlier drafts. One anonymous referee provided much helpful criticism of an earlier version of this paper.
References Andrew, R.J., 1963. The origin and evolution of the calls and facial expressions of the primates. Behaviour, 20: l- 109. Bauers, K. and Snowdon, C.T., 1990. Discrimination of chirp vocalizations in the cotton-top tamarin. Am. J. Primatol., 21: 53-60. Boinski, S., 1991. The coordination of spatial position: a field study of the vocal behaviour of adult female squirrel monkeys. Anim. Behav., 41: 89-102. Box, H.O., 1977. Quantitative data on the carrying of young captive monkeys (C’nl/ithrixjucch~~~) by other members of their family groups. Primates, 18: 475-484. Caine, N.G. and Stevens, C., 1990. Evidence for a ‘monitoring call’ in red-bellied tamarins. Am. J. Primatol., 22: 25 I-262. Emlen, ST., 1991. Cooperative breeding in birds and mammals. In: J.R. Krebs and N.B. Davies (Editors), Behavioural Ecology. Blackwell Scientific Publications, Oxford, pp. 301-337. Engel, C., 1985. Observations on the interaction between adult infant-carrying animals and group members without rearing experience in the common marmoset, Cdirhrix jucchus. Folia Primatol., 45: 225-235. Epple, G., 1968. Comparative studies on vocalization in marmoset monkeys (Hupalidue). Folia Primatol., 8: I-40. Ferrari, S.F., 1992. The care of infants in a wild marmoset (Cullithrix,flal,ic~~~) group. Am. J. Primatol., 26: 109-I 18. Fischer, J., Hammerschmidt, K. and Todt, D., 1995. Factors affecting acoustic variation in barbary-macaque (Macacu syluunus) disturbance calls. Ethology, 101: 5 l-66. Godfray, H.C.J., 1991. Signalling of need by offspring to their parents. Nature, 352: 328-330. Goedeking, P. and Immelmann, K., 1986. Vocal cues in cotton-top tamarin play vocalizations. Ethology, 73: 219-224. Goldizen, A.W., 1990. A comparative perspective on the evolution of tamarin and marmoset social systems. Int. J. Primatol., 11: 63-83. Gouzoules, H. and Gouzoules, S., 1990. Body size effects on the acoustic structure of pigtail macaques (Mncacn nentestn’nu) screams. Ethology, 85: 324-334. Green, S., 1975. Variation of vocal pattern with social situation in the japanese monkey (M~~cucu~~scat~): a field study. In: L.A. Rosenblum (Editor), Primate Behavior. Academic Press. New York, NY, pp. l-103 Hammerschmidt, K., Ansorge, V. and Fischer, J., 1994a. Age-related variations in the vocal repertoire of barbary macaques. In: J.J. Roeder, B. Thierry, J.R. Anderson and N. Herrenschmidt (Editors), Current Primatology II. Universite Louis Pasteur, Strasbourg, pp. 287-295. Hammerschmidt, K., Ansorge, V., Fischer, J. and Todt, D., 1994b. Dusk calling in barbary macaques (Mucuca .r$~‘nnu.s): demand for social shelter. Am. J. Primatol., 32: 277-289. Huhsch, H. and Todt, J., 1996. Rules of parameter variation in homotype series of birdsong can indicate a ‘sollwert’ significance. Behav. Process., 38: 175- 182. Ingram, J.C., 1977. Interactions between parents and infants, and the development of independence in the common marmoset (Cullithrix jucchm). Anim. Behav., 25: 8 1 I-827. Jiirgens, U., 1979. Vocalizations as an emotional indicator: a neuroethological study in the squirrel monkey. Behaviour, 69: 80-l 17. McGrew, W.C. and McLuckie, E.C., 1986. Philopatry and dispersion in the cotton-top tamarin, Sug~linus f0.i o&pus: an attempted laboratory simulation. Int. J. Primatol., 7: 401-422. Morton, E.S., 1977. On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Am. Nat., 11 I: 855-869. Newman, J.D., 1995. Vocal ontogeny in macaques and marmosets: convergent and divergent lines of development. In: E. Zimmermann, J.D. Newman and U. Jiirgens (Editors), Current Topics in Primate Vocal Communication, Plenum Press, New York, NY, pp. 73-97.
S. Geiss. L. Schrzrder/ Brhmiouml Processes 38 CJYY61 183-l YJ
191
Newman, J.D. and Goedeking, P., 1992. Noncategorical vocal communication in primates: the example of common marmoset phee calls. In: H. Papousek, U. Jurgens and M. Papousek (Editors), Nonverbal Vocal Communication, Cambridge University Press, Cambridge. Norcross, J.L., Newman, J.D. and Fitch, W.. 1994. Responses to natural and synthetic phee calls by common marmosets (Cu//ifhri.wjaccllus). Am. J. Primatol., 33: l-29. Price, E.C., 1991. Competition to carry infants in captive families of cotton-top tamarins (Suguinus m&pus). Behaviour, I 18: 66-88. Riechelmann. C., Hultsch, H. and Todt. D., 1994. Early development of social relationships in barbary macaques (Mucuca .rvl~~an~ls):trajectories of alloparental behaviour during an infant’s first three month of life. In: J.J. Roeder, B. Thierry, J.R. Anderson and N. Herrenschmidt (Editors), Current Primatology 11. Universite Louis Pasteur, Strasbourg, pp. 279-286. Schrader, L. and Todt, D., 1993. Contact call parameters covary with social context in common marmosets, Cdlithrix j. jucchus. Anim. Behav.. 46: 102661028. Schrader, L. and Hammerschmidt, K., 1996. Computer-aided analysis of acoustic parameters in animal vocalizations: a multi-parametric approach. Bioacoustics, in press. Snowdon, C.T. and Pola, Y.V., 1978. Interspecific and intraspecific responses to synthesized pygmy marmoset vocalizations. Anim. Behav., 26: 192-206. Snowdon, CT. and Cleveland, J., 1980. Individual recognition of contact calls by pygmy marmosets. Anim. Behav., 28: 7 17-727. Snowdon. CT. and Cleveland, J., 1984. ‘Conversations’ among pygmy marmosets. Am. J. Primatol., 7: 15-20. Snowdon, CT., Cleveland, J. and French, J.A., 1983. Responses to context- and individual-specific cues in cotton-top tamarin long calls. Anim. Behav., 31: 92- 101. Stevenson, M.F. and Rylands, A.B. (1986). The marmosets. genus Cdithrix. In: A.F. Coimbra-Filho and R.A. Mittermeier (Editors). Ecology and Behavior of Neotropical Primates II. Academia Brasileira de Ci&ncias, Rio de Janeiro, pp. 131-222. Sussman, R.W. and Garber, P.A.. 1987. A new interpretation of the social organization and mating system of the callitrichidae. Int. J. Primatol., 8: 73392. Tardif, S.D., 1994. Relative energetic cost of infant care in small-bodied neotropical primates and its relation to infant-care patterns. Am. J. Primatol., 34: 1333143. Tardif, S.D., Carson, R.L. and Gangaware, B.L., 1992. Infant-care behavior of non-reproductive helpers in a communal-care primate, the cotton-top tamarin fSuguims m&pus). Ethology, 92: 155-167. Terborgh, J. and Goldizen, A.W., 1985. On the mating system of the cooperatively breeding saddle-backed tamarin (S~lguinus~~.scicol[is). Behav. Ecol. Sociobiol., 16: 293-299. Todt. D., 1988. Serial calling as a mediator of interaction processes: crying in primates. In: D. Todt, P. Goedeking and D. Symmes (Editors), Primate Vocal Communication, Springer, Berlin, pp. 888107. Todt, D., 1996. The dynamic of crying and its interactional role: phasic versus tonic components. In: B. Lester, J.D. Newman and F. Pederson (Editors), Social and Biological Aspects of Infant Crying. Plenum Press, New York, NY. Todt, D. and Hultsch, H., 1996. Functional aspects of parameter variation in serial vocalizations. In: J. Supriatna (Editor), Proceedings of the XXth Congress of the International Primatology Society, Djakarta. Weary, D.M. and Fraser, D., 1995. Calling by domestic piglets: reliable signals of need? Anim. Behav., 50: 1047-1055. Winter, M., 1977. Some aspects of the ontogeny of vocalizations of hand-reared common marmosets. In: H. Rothe, H.J. Wolters and J.P. Hearn (Editors), Biology and Behaviour of Marmosets. Eigenverlag Rothe, Giittingen, pp. 127-139. Winter, M. and Rothe, H., 1979. Darstellung des Lautrepertoires handaufgezogener WeissbuschelPffchen (Cdithrix j. jacchus) unter besonderer Beriicksichtigung der tliessenden Ubergange zwischen den einzelnen Lautgruppen. Primates, 20: 259-276.
Behavioural Processes 38 (I 996) 183- 19I
Temporal and structural features of infant calls in relation to caregiving behaviour in common marmosets, Callithrix j. jacchus’ Stefan Geiss, Lars Schrader Institutfir
Verhaltensbinlogiu,
*
FU Berlin, Haderslebener Strabe 9, D-12163 Berlin, Germany Accepted 2 April 1996
Abstract The role of infants in the communal rearing system of marmosets and tamarins has received little attention although their demands may not be complied by inadequate helpers. As acoustic signalling plays an important role in their social communication, it is expected to be an effective way for infants to signal their demand for care. As a first approach, this study focussed on the use and quality of ‘tsik’ calls given by infants of common marmosets (Cullirhrix j. jucchus) in the context of caregiving. The acoustic and non-acoustic behaviour of a group of common marmosets were recorded during the first two weeks of the life of two infants (twins). Vocalizations were classified, and the structure of the infants’ ‘tsik’ calls was quantified by measuring specific signal parameters. Infants gave ‘tsik’ calls in close temporal relation to caregiving behaviour. Specific parameters covaried with the subsequent behaviour of potential caretakers. Values of call duration, start frequency, peak frequency, and range were lower when infants’ calls were followed by no reaction or an approach of group members, whereas these parameters showed higher values when followed by a transfer of infants. Our results suggest that the actual demand of infants is encoded in the variations of ‘tsik’ calls. Keywords:
Acoustic parameter;
Caregiving
behaviour;
Common marmoset;
Communal rearing system; Vocalization
1. Introduction In the communal
rearing
system
of marmosets
and tamarins
(Callitrichidae)
only
the dominant
female reproduces, but all other group members are involved in carrying and taking care of the infants (Goldizen, 1990; Stevenson and Rylands, 1986; Sussman and Garber, 1987). The advantages to the mother resulting from this social system are quite obvious. Usually she gives birth to twins, the
* Corresponding author. ’ Based on a contribution to the Bioacoustics and Man’ (Merbitz, Germany, 1995).
Workshop
0376.6357/96/$15.00 Copyright 0 1996 Elsevier Science P/I SO376-6357(96)00022-S
‘Numerical Methods for the Study of Vocalization
B.V. All
rights reserved.
in Animals
weight of which is almost 20% of the mothers weight. Carrying the infants impairs foraging in a period of time when her metabolism is greatly accelerated by demands of lactation (Tardif, 1994; Terborgh and Goldizen, 1985). Adult males are the primary infant carriers, and the extent of infant-care of other group members, mostly siblings of the newborns, increases with age (Ingram. 1977; Tardif et al., 1992; Terborgh and Goldizen, 1985). Although often more than one adult male may be reproductively active, adult males may profit directly in rearing their potential offsprings (Terborgh and Goldizen, 1985), and they may influence future female mate choice in demonstrating their skills in infant care (Ferrari, 1992; Price, 1991). The other group members can profit by enhancing their inclusive fitness by kin selection, acquiring experience in parental behaviour. developing cooperative relationships or increasing their chance of inheriting the territory later on (Emlen, 1991; McGrew and McLuckie, 1986; Price, 1991; Terborgh and Goldizen, 1985). Most of the studies on the communal rearing system in marmosets and tamarins have focussed on the caregivers, whereas the role of infants has received little attention. However, the need of infants is a crucial factor in the evolution of this social system and should be reflected in the social interactions between infants and caregivers. One main interest of infants is to obtain enough milk from their mother. Hence, it is crucial for them to be transferred to their mother whenever they need food. If their mother does not take the infants by herself in regular intervals, the infants should be able to signal their demand. As infants are quite dependent and immobile they should be interested in receiving care from experienced group members. Handling by young and unexperienced group members may pose potential risks of inadequate care for the infants (Engel. 1985; Price, 199 1; Riechelmann et al., 1994). Competition between group members to carry infants may also impair the quality of care. Furthermore, adults may intervene attempts of younger group members to retrieve infants (Price, 1991). Hence the lower proportion of young group members that help in infant care may reflect the attempt of experienced adults to reduce the risk of inadequate care. Thus. again, infants should be able to signal that they are treated inadequately. Acoustic signalling plays an important role in communication between and within groups of marmosets and tamarins (Boinski. 1991; Caine and Stevens, 1990; Schrader and Todt, 1993; Snowdon et al., 1983; Snowdon and Cleveland, 1984). Due to the dense vegetation of South American rain forests, visual contact is often restricted. According to these constraints on communication facial expressions in New World monkeys are not well developed compared to those in Old World monkeys (Andrew, 1963). Hence, acoustic signalling is expected to be a more effective way for infants to signal their demand to potential caregivers. The aim of this study was to investigate the role of acoustic signalling in caregiving. We focussed on vocalizations of infants to investigate whether and how the behaviour of group members covaries with infants’ signalling behaviour. Such covariations would indicate that infants are able to signal their demand acoustically. We focussed on the following specific questions: (a) do infants of common marmosets use specific vocal patterns in the context of caretaking?; (b) are there temporal correlations between specific infant vocalizations and the behaviour of caregivers?; and (c> how do characteristics of infants’ calls covariate with specific behaviours of caregivers? 2. Materials and methods We studied a family group of 9 common marmosets ( Callithrix j. jacchus) ( 1 adult female, 2 adult males, 2 sub-adult males, 2 juvenile males, 2 infants) housed together in an indoor wire meshed cage
S. Griss.
L. S~,hrud~r/Behal,iourcrl
Pmcessr.~
38 IIYY6I
183-191
185
(3.5 X 2.5 X 2 m) enriched with branches and nest boxes. In order to optimize acoustic conditions, room walls were covered with unechoic material. Subjects were observed daily during the first two weeks after the birth of the youngest infants. Observation sessions were distributed randomly over the activity phase of the group, and on each day 2 to 4 observation sessions were conducted. A total of 30 h were recorded, including 78 transfers of infants from one group member to another one. Social interactions (approaching , grooming, grasping, olfactory control, tugging and transfer) shown by group members directed to infants as well as suckling were recorded continuously with a mini computer (Atari portfolio; software: BEHAVIOR 2.3, developed by Kurt Hammerschmidt and Lars Schrader). Vocalizations were recorded with a tape recorder (REVOX PR 99, 7.5 cm/s; Sennheiser ME 80). Whenever we saw that a given subject, and especially an infant, was vocalizing, this was commented on the second channel of tape recorder. We used 3 subsets of the total sample to analyse vocalizations. As our criteria to select these subsamples depended on the respective step of analysis, they are explained in the results. Vocalizations were classified by visual inspection of spectrograms, following the definition by Winter and Rothe (1979) and using software for real-time spectrograms CRTS, Engineering Design, Boston, MA, USA). As a result of an initial analysis of vocal patterns, we focussed on the ‘tsik’ calls given by the infants. As vocal patterns of infants were highly variable (cf., Winter, 1977) only calls with an up-sweep from start frequency to peak frequency followed by a down-sweep to end-frequency were defined as ‘tsik’ calls. Intermediate forms of ‘tsik’ calls with other call types were not considered. Due to their different pitch, infants’ ‘ tsik’ calls could be distinguished unambiguously from ‘tsik’ calls of other subjects. Parameters of ‘tsik’ calls were measured using RTS (frequency range: 16 kHz, frequency resolution: 79 Hz, time resolution: 7 ms). We quantified the structure of ‘tsik’ calls by using the following parameters (see also Fig. 1): (1) start frequency, (2) peak frequency, (3) end frequency, (4) duration, (5) frequency range (i.e., peak frequency-end frequency), (6) frequency increase (i.e., peak frequency-start frequency), (7) frequency decrease (i.e., peak frequency-end frequency), (8) time-structure (i.e., duration of frequency increase/duration of frequency decrease), (9) frequency-structure (i.e., frequency increase/frequency decrease), ( 10) frequency decrease per time (i.e., frequency decrease/duration of frequency decrease). We used SPSS for Windows 6.0 for statistical analysis. Univariate covariations between rearing contexts and acoustic parameters were tested with a Kruskal-Wallis one-way ANOVA. Discriminant
1
2
3 Time [s]
Fig. 1. Spectrogram of a series of five ‘tsik’ calls given by an infant of common marmosets. Signal parameters measured in spectrograms were (a) start frequency, (b) peak frequency, (c) end frequency, and (d) duration.
analysis was applied to check whether vocalizations could be distinguished statistically between sub-contexts (defined below). The discriminant analysis compares multivariate patterns resulting from any interaction of variables. It provides a classification procedure that assigns each call either to its appropriate group (correct assignment) or to another group (incorrect assignment). Furthermore, it calculates a rank order in which parameters are important for distinguishing among groups.
3. Results All group members took part in carrying the infants during their first two weeks of life. In total, the mother carried one or both infants in 19% of cases, the dominant male in 39%, the other adult male in 17%, the two sub-adults in 23%, and the two juveniles in 3% of all observed instances. To calculate an overall budget for vocalizations we randomly selected a sample of 1 h from our observation time of 30 h (sample (I)). We excluded phases in which high vocal activity were most likely caused by external stimuli (e.g., sudden appearance of a bird in front of the window) and phases with no activity (e.g., the whole group was resting) from analysis. This sample (I) included 2500 vocalizations. Within sample (I) 68% of calls could be classified as ‘phee’ calls, 12% as ‘tsik’ calls, 10% as ‘qua+ calls, 7% as ‘twitter’ calls, and 3% as other call types (cf., Winter and Rothe, 1979). 93% of the ‘tsik’ calls in this sample were uttered by the two infants. In the next step of analysis we focussed on the interactions between group members and infants. These interactions included approaches of group members to the infants as well as transfers. As a result of the preceding analysis, we only included interactions during which ‘tsik’ calls were given by infants. This sample (11) again was selected randomly from the overall observation of 30 h. In total, 6 h were covered, and 2310 ‘tsik’ calls of infants and 28 transfers were included. 58% of the infants’ ‘tsik’ calls were given within 2 min before infants were transferred. The remaining 42% of ‘tsik’ calls were most often also followed by a reaction of group members (e.g., approach), but were not followed by a transfer. When ‘tsik’ calls were given by infants without a following transfer call rate of infant ‘tsik’ calls was 3.1 calls per min. In contrast, call rate increased to 26.4 calls per min in the time window of 2 min before a transfer took place. In a third step we analyzed the relation between infant ‘tsik’ calls and the succeeding behaviour of group members in more detail. Within 2 min after the onset of infant ‘tsik’ calls we defined four behavioural contexts, based on the behaviour of group members: (A) a group member approached but did not take the infant; (B) a group member approached and took the infant; (Cl a group member immediately took the infant as contact had already been established; (X) ‘tsik’ calls were not followed by any reaction of group members within these 2 min. This sample (III) was identical to sample (II), but in order to test for covariations between call structure and behavioural contexts, we selected 633 ‘tsik’ calls from the total of 2310 to measure signal parameters. All call parameters measured, except the frequency decrease per time, covaried significantly with the different behavioural contexts (Kruskal-Wallis H test, P < 0.001). Fig. 2 shows an example of four parameters. The values of start frequency, peak frequency, frequency range and duration increased from context (X) over context (A) to context (B), whereas the values in context (C) were at least lower than in context (B). The discriminant analyses showed that the acoustic structure of calls from the 4 sub-contexts clearly differed. 58% of calls were correctly classified (random assignment 25%) (Table 1). Best
187
Start
Frequency
Peak Frequency
12
l3 1
11
*
2 y 10 z
t
Y
a)
I
8
A
+ +
*
7’X
t
%ll 5 3 z z lo-
5 z 9
E
.
p 12 -
B
C
b)s-
X
A
8
C
Subcontext
Frequency
Range
Call Duration
t
+
t t cl
3'X
A
B
C
cl)
so
Subcontext
X
A 6 Subcontext
C
Fig. 2. Means and standard error of the (a> start frequency, (b) peak frequency, (c) frequency range, and (d) call dLIration of ‘tsik’ calls given by infants. Sub-contexts were defined due to the behavioural reaction of group members after onset of infant calting: (X> no reaction (n = 1401, (A) approach (n = 1401, (B) approach and transfer (n = 331), and (C) immediate transfer (11= 22).
predictor variables were (I) start frequency, (2) peak frequency, (3) frequency range, and (4) duration (Fig. 2). When contexts were combined in a context ‘transfer’ (context B -t context C) and a second context ‘no transfer’ (context A + context X), 92% of calls were classified correctly (random assignment 50%) (Table 1).
Table 1 Result of discriminant
anal-&+
Actual sub-context
X: A: B: C:
No reaction Approach Approach with transfer Transfer
Predicted membership
to sub-context
X: No reaction
A: Approach
B: Approach with transfer
C: Transfer
n
64% (89) 34% (48) 2% (6) 0% (0)
30% (42) 56% (79) 7% (22) 0% (0)
4% (6) 6% (8) 54% (179) 18% (4)
2% (3) 4% (5) 38% (124) 82% (18)
140 140 331 22
Infants’ ‘tsik’ calls were classified in the four sub-contexts on the basis of measured signal parameters. assignment and the total number of assigned calls (in parentheses) is shown.
The percentages
of
188
4. IXscussion Our results provide the first evidence that the ‘tsik’ calls of common marmoset infants may contain information about their actual demand for care. The performance of infants’ ‘t&k calls was associated with social interactions between group members and infants. In particular, we found temporal relations between the onset of the infants ’ ‘tsik’ calls and the succeeding behaviour of group members. Within 2 min after the infants started calling, most often a group member approached or took the infant. Moreover, the type of reaction (no reaction, approach, approach and transfer, immediate transfer) covaried with certain structural features of the infants’ ‘tsik’ calls. Although our sample size is still relatively small, the results suggest that infants have the potential to play an active role in caregiving behaviour. Our data on the percentage of time the different group members carried the infants are in line with observations of other studies on captive common marmosets. In the first two weeks the infants were carried mainly by their mother and the adult males, less by the two sub-adults and the two juveniles (cf., Box, 1977; Engel, 198.5; Ingram, 1977). This indicates that caregiving behaviour of the group we studied was similar to that in other groups of captive common marmosets. ‘Tsik’ calls were given predominantly by infants and in close temporal relation to caregiving behaviour. The use of specific vocal patterns by infants in relation to caregiving is well known in humans and in nonhuman primates. In human babies as well as in infants of Old World monkeys these vocal patterns most often consist of cry series (for reviews, see Todt, 1988, 1996). Cries are complex vocal patterns, characterized by large frequency ranges, noisy and shrill frequency features, and a high variability of acoustic parameters within a series of crying. In contrast, ‘tsik’ calls of common marmosets have a rather simple acoustic tonal structure. However, common marmosets also produce another call type, the squeal call or ‘qu%-r’ call (Winter and Rothe, 19791, which has similar signal characteristics as the cries of human babies and of nonhuman primates’ infants. In common marmosets there are only a few studies about the use of vocalizations of infants or about vocal ontogeny (cf., Newman, 1995). Winter (1977) described infant vocalizations on the day after birth and found four call types which were very variable in structure and were uttered in no constant sequence. In addition, intermediate patterns of call types occurred regularly. Call types could not be related to specific situations. Instead, they seemed to indicate unspecific distress. Also Epple (1968) noted that, with increasing distress, infants give series of ‘tsik’ call, twitters and squeals. Our observations suggest that the squeals were given predominantly by the two juvenile males during their mostly unsuccessful and dismissed attempts to take the infants from older group members. Infants gave ‘tsik’ calls much more often than other group members, although call sequences could include not only ‘tsik’ calls but also other vocal patterns. Adult common marmosets give ‘tsik’ calls in aversive situations, for example when mobbing a predator (Epple, 19681, if unfamiliar persons approach their cage, or when subjects are caught for physical examination (personal observations). Hence, ‘tsik’ calls might indicate a senders’ discomfort or distress. Our results indicate that with the quality of infants’ ‘ tsik’ calls the behaviour of possible caregivers covaried. Lower values of call duration, start frequency, peak frequency, and range in the infants’ ‘tsik’ calls were followed by no reaction or an approach of group members, while ‘tsik’ calls with higher values of these parameters were followed by a transfer of infants. Discriminant analyses showed that due to their structure these v~iations of infants’ ‘tsik’ calls could be assigned clearly to the type of behaviour that was shown by group members following the onset of infants’ calling.
Since the investigation by Green ( 1975) on vocalizations of Japanese monkeys ( Macacu f~scata), an increasing number of studies have shown that even subtle variations of a given call type may covary with social context and thus may reflect the internal state of sender. Information about the quality and the level of internal state can be deduced from temporal changes of specific par~eters (Todt, 1996; Todt and Hultsch, 1996, see also Hultsch and Todt, 1996). Nowadays computer-aided analysis of acoustic signals allows for exact quantification of such variation of vocalizations (Schrader and Hammerschmidt, in press). For the ‘phee’ call of common marmosets it could be shown in separation experiments that call duration, frequency. frequency range and amplitude increased with decreasing sensory information about mates (Schrader and Todt, 1993). Furthermore, the frequency as well as the call duration changed with increasing time of separation (Newman and Goedeking. 1992). The authors suggested that these changes may reflect the changing arousal of the sender. In cotton-top tamarins (Saguirtus oedipus) the instability of fundamental frequency was found to correlate with playful interactions (Goedeking and Immelmann, 1986). In vocalizations of squirrel monkeys (Suivniri sciureus), Jiirgens (1979) found a positive correlation between aversiveness of calls and the total frequency range in non-harmonic, noisy calls. In high-pitched harmonic calls he found correlations with the pitch of fundamental frequency and irregularity of frequency course. For Old World monkeys, covariations between frequency and frequency range and the quality of aggressive interactions were found in the screams of pigtail macaques (~ffc~~~ ~?e~~~~~~~z~) (Gouzoules and Gouzoules, 1990). In the disturbance calls of barbary macaques ( Mucaca s~lucrnus) time as well as frequency characteristics within call series shifted gradually (Fischer et al., 19951, indicating a change of internal state. in summary, the findings described above are in line with the motivation-structural rules by Morton (1977) who hypothesized a general relationship between physical structures of sounds and the motivation underlying their use. Regarding his model the ‘tsik’ calls of common marmosets might indicate a high level of fear or submission, combined with an increasing hostility. Thus. the acoustic quality of infants’ ‘tsik’ calls might reflect the arousal or emotional state which presumably is affected by the quality of care they receive. Hence infants might be able to signal their demand for a change in care. The possibility that receivers of such signals are able to distinguish subtle variations in signal structure could be shown for common marmosets (Norcross et al., 19941, cotton-top tamarins (Bauers and Snowdon, 19901, and pygmy marmosets (C&rella pq‘gmeae) (Snowdon and Cleveland, 1980; Snowdon and Pola, 1978). That vocalizations may reliably signal the need of offsprings was demonstrated with a matheInatical model by Godfray ( 1991). Hammerschmidt et al. ( 1994a,b) investigated the dusk calling in barbary macaques. At dusk, juveniles often utter heterotype series of vocalizations that last until the callers have formed sleeping clusters with other individuals. Here, too, the vocalizations might indicate their social demand. Weary and Fraser ( 1995) found in domestic pigs (Sus SCK$ ~~u~esri~a) that vocalizations of piglets in poor condition of nutrition had higher call duration and frequency parameters than piglets in good condition. They concluded that the piglets’ need was encoded in these acoustic features. Taking the findings of other studies into account, our results in common marmosets suggest that the actual demand for care is potentially encoded in variations of infants’ ‘tsik’ calls. Although the data were gathered from only one family group, our study indicates that infants may play an active role in the communal rearing system of marmosets and tamarins. Further studies may focus on signalling in dependence of the individual identity of different caregivers.
190
S. Geiss. L. Schmder/Behnc,iourul
Processrs 38 (1996) 183-191
Acknowledgements We would like to thank Jiirg Bijhner, Julia Fischer, Kurt Hammerschmidt, Marc Naguib, Cord Riechelmann and Dietmar Todt for stimulating discussions and critical comments on earlier drafts. One anonymous referee provided much helpful criticism of an earlier version of this paper.
References Andrew, R.J., 1963. The origin and evolution of the calls and facial expressions of the primates. Behaviour, 20: l- 109. Bauers, K. and Snowdon, C.T., 1990. Discrimination of chirp vocalizations in the cotton-top tamarin. Am. J. Primatol., 21: 53-60. Boinski, S., 1991. The coordination of spatial position: a field study of the vocal behaviour of adult female squirrel monkeys. Anim. Behav., 41: 89-102. Box, H.O., 1977. Quantitative data on the carrying of young captive monkeys (C’nl/ithrixjucch~~~) by other members of their family groups. Primates, 18: 475-484. Caine, N.G. and Stevens, C., 1990. Evidence for a ‘monitoring call’ in red-bellied tamarins. Am. J. Primatol., 22: 25 I-262. Emlen, ST., 1991. Cooperative breeding in birds and mammals. In: J.R. Krebs and N.B. Davies (Editors), Behavioural Ecology. Blackwell Scientific Publications, Oxford, pp. 301-337. Engel, C., 1985. Observations on the interaction between adult infant-carrying animals and group members without rearing experience in the common marmoset, Cdirhrix jucchus. Folia Primatol., 45: 225-235. Epple, G., 1968. Comparative studies on vocalization in marmoset monkeys (Hupalidue). Folia Primatol., 8: I-40. Ferrari, S.F., 1992. The care of infants in a wild marmoset (Cullithrix,flal,ic~~~) group. Am. J. Primatol., 26: 109-I 18. Fischer, J., Hammerschmidt, K. and Todt, D., 1995. Factors affecting acoustic variation in barbary-macaque (Macacu syluunus) disturbance calls. Ethology, 101: 5 l-66. Godfray, H.C.J., 1991. Signalling of need by offspring to their parents. Nature, 352: 328-330. Goedeking, P. and Immelmann, K., 1986. Vocal cues in cotton-top tamarin play vocalizations. Ethology, 73: 219-224. Goldizen, A.W., 1990. A comparative perspective on the evolution of tamarin and marmoset social systems. Int. J. Primatol., 11: 63-83. Gouzoules, H. and Gouzoules, S., 1990. Body size effects on the acoustic structure of pigtail macaques (Mncacn nentestn’nu) screams. Ethology, 85: 324-334. Green, S., 1975. Variation of vocal pattern with social situation in the japanese monkey (M~~cucu~~scat~): a field study. In: L.A. Rosenblum (Editor), Primate Behavior. Academic Press. New York, NY, pp. l-103 Hammerschmidt, K., Ansorge, V. and Fischer, J., 1994a. Age-related variations in the vocal repertoire of barbary macaques. In: J.J. Roeder, B. Thierry, J.R. Anderson and N. Herrenschmidt (Editors), Current Primatology II. Universite Louis Pasteur, Strasbourg, pp. 287-295. Hammerschmidt, K., Ansorge, V., Fischer, J. and Todt, D., 1994b. Dusk calling in barbary macaques (Mucuca .r$~‘nnu.s): demand for social shelter. Am. J. Primatol., 32: 277-289. Huhsch, H. and Todt, J., 1996. Rules of parameter variation in homotype series of birdsong can indicate a ‘sollwert’ significance. Behav. Process., 38: 175- 182. Ingram, J.C., 1977. Interactions between parents and infants, and the development of independence in the common marmoset (Cullithrix jucchm). Anim. Behav., 25: 8 1 I-827. Jiirgens, U., 1979. Vocalizations as an emotional indicator: a neuroethological study in the squirrel monkey. Behaviour, 69: 80-l 17. McGrew, W.C. and McLuckie, E.C., 1986. Philopatry and dispersion in the cotton-top tamarin, Sug~linus f0.i o&pus: an attempted laboratory simulation. Int. J. Primatol., 7: 401-422. Morton, E.S., 1977. On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Am. Nat., 11 I: 855-869. Newman, J.D., 1995. Vocal ontogeny in macaques and marmosets: convergent and divergent lines of development. In: E. Zimmermann, J.D. Newman and U. Jiirgens (Editors), Current Topics in Primate Vocal Communication, Plenum Press, New York, NY, pp. 73-97.
S. Geiss. L. Schrzrder/ Brhmiouml Processes 38 CJYY61 183-l YJ
191
Newman, J.D. and Goedeking, P., 1992. Noncategorical vocal communication in primates: the example of common marmoset phee calls. In: H. Papousek, U. Jurgens and M. Papousek (Editors), Nonverbal Vocal Communication, Cambridge University Press, Cambridge. Norcross, J.L., Newman, J.D. and Fitch, W.. 1994. Responses to natural and synthetic phee calls by common marmosets (Cu//ifhri.wjaccllus). Am. J. Primatol., 33: l-29. Price, E.C., 1991. Competition to carry infants in captive families of cotton-top tamarins (Suguinus m&pus). Behaviour, I 18: 66-88. Riechelmann. C., Hultsch, H. and Todt. D., 1994. Early development of social relationships in barbary macaques (Mucuca .rvl~~an~ls):trajectories of alloparental behaviour during an infant’s first three month of life. In: J.J. Roeder, B. Thierry, J.R. Anderson and N. Herrenschmidt (Editors), Current Primatology 11. Universite Louis Pasteur, Strasbourg, pp. 279-286. Schrader, L. and Todt, D., 1993. Contact call parameters covary with social context in common marmosets, Cdlithrix j. jucchus. Anim. Behav.. 46: 102661028. Schrader, L. and Hammerschmidt, K., 1996. Computer-aided analysis of acoustic parameters in animal vocalizations: a multi-parametric approach. Bioacoustics, in press. Snowdon, C.T. and Pola, Y.V., 1978. Interspecific and intraspecific responses to synthesized pygmy marmoset vocalizations. Anim. Behav., 26: 192-206. Snowdon, CT. and Cleveland, J., 1980. Individual recognition of contact calls by pygmy marmosets. Anim. Behav., 28: 7 17-727. Snowdon. CT. and Cleveland, J., 1984. ‘Conversations’ among pygmy marmosets. Am. J. Primatol., 7: 15-20. Snowdon, CT., Cleveland, J. and French, J.A., 1983. Responses to context- and individual-specific cues in cotton-top tamarin long calls. Anim. Behav., 31: 92- 101. Stevenson, M.F. and Rylands, A.B. (1986). The marmosets. genus Cdithrix. In: A.F. Coimbra-Filho and R.A. Mittermeier (Editors). Ecology and Behavior of Neotropical Primates II. Academia Brasileira de Ci&ncias, Rio de Janeiro, pp. 131-222. Sussman, R.W. and Garber, P.A.. 1987. A new interpretation of the social organization and mating system of the callitrichidae. Int. J. Primatol., 8: 73392. Tardif, S.D., 1994. Relative energetic cost of infant care in small-bodied neotropical primates and its relation to infant-care patterns. Am. J. Primatol., 34: 1333143. Tardif, S.D., Carson, R.L. and Gangaware, B.L., 1992. Infant-care behavior of non-reproductive helpers in a communal-care primate, the cotton-top tamarin fSuguims m&pus). Ethology, 92: 155-167. Terborgh, J. and Goldizen, A.W., 1985. On the mating system of the cooperatively breeding saddle-backed tamarin (S~lguinus~~.scicol[is). Behav. Ecol. Sociobiol., 16: 293-299. Todt. D., 1988. Serial calling as a mediator of interaction processes: crying in primates. In: D. Todt, P. Goedeking and D. Symmes (Editors), Primate Vocal Communication, Springer, Berlin, pp. 888107. Todt, D., 1996. The dynamic of crying and its interactional role: phasic versus tonic components. In: B. Lester, J.D. Newman and F. Pederson (Editors), Social and Biological Aspects of Infant Crying. Plenum Press, New York, NY. Todt, D. and Hultsch, H., 1996. Functional aspects of parameter variation in serial vocalizations. In: J. Supriatna (Editor), Proceedings of the XXth Congress of the International Primatology Society, Djakarta. Weary, D.M. and Fraser, D., 1995. Calling by domestic piglets: reliable signals of need? Anim. Behav., 50: 1047-1055. Winter, M., 1977. Some aspects of the ontogeny of vocalizations of hand-reared common marmosets. In: H. Rothe, H.J. Wolters and J.P. Hearn (Editors), Biology and Behaviour of Marmosets. Eigenverlag Rothe, Giittingen, pp. 127-139. Winter, M. and Rothe, H., 1979. Darstellung des Lautrepertoires handaufgezogener WeissbuschelPffchen (Cdithrix j. jacchus) unter besonderer Beriicksichtigung der tliessenden Ubergange zwischen den einzelnen Lautgruppen. Primates, 20: 259-276.