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Degree of social contact affects the emission of food calls in the common marmoset (Callithrix jacchus).

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American Journal of Primatology 59:21–28 (2003)
RESEARCH ARTICLE
Degree of Social Contact Affects the Emission of Food
Calls in the Common Marmoset (Callithrix jacchus)
AUGUSTO VITALE,1,n MICHELA ZANZONI1, ARMELLE QUEYRAS1, and FLAVIA
CHIAROTTI2
1
Section of Comparative Psychology, Laboratorio di Fisiopatologia di Organo e di Sistema,
Istituto Superiore di Sanità, Rome, Italy
2
Section of Behavioral Pathophysiology, Laboratorio di Fisiopatologia di Organo di
Sistema, Istituto Superiore di Sanità, Rome, Italy
The aim of this study was to investigate whether the emission of food
calls in common marmosets (Callithrix jacchus) is influenced by different
social contexts. Food calls are emitted by this species only in the presence
of preferred food. If these calls have any communicative function, it may
be that individuals produce food calls in order to call family mates toward
the food source. If this is the case, the number of calls produced should
vary in accordance with the number of family mates present at the
moment of the discovery of the food, i.e., the fewer family mates nearby,
the more food calls are emitted. This hypothesis was tested with five pairs
of common marmosets, by recording the number of food calls emitted in
four experimental conditions: 1) isolation: completely isolated from
the family mates; 2) visual isolation: separated by a wooden panel from
the family mates; 3) visual contact: separated by a wire-mesh from the
family mates; and 4) physical interaction: together with the family
mates. The results show that the proportion of intervals during which
food calls were produced by the pairs was significantly different in
the four experimental conditions. It decreased from the isolation and
visual isolation condition, through the visual contact condition, reaching
the lowest value in the physical interaction condition. The variation
observed in the proportion of intervals during which food calls were
emitted, in relation to different social contexts, is an indication in favor
of the communicative function of this vocalization. Am. J. Primatol.
59:21–28, 2003.
r 2003 Wiley-Liss, Inc.
Key words: Callithrix jacchus; common marmoset; food calls; social
context; vocalizations
n
Correspondence to: Augusto Vitale, Section of Comparative Psychology, Laboratorio di
Fisiopatologia di Organo e di Sistema, Istituto Superiore di Sanità, Viale Regina Elena 299,
00161 Rome, Italy. E-mail: vitale@iss.it
Received 31 March 2002; revision accepted 22 October 2002
DOI: 10.1002/ajp.10060
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2003 Wiley-Liss, Inc.
22 / Vitale et al.
INTRODUCTION
Food calls can be generally defined as: ‘‘vocalisations uttered by an animal
upon encountering a food source’’ [Caine et al., 1995, p. 53]. Such vocalizations
have been recorded in different species of nonhuman primates. Among New
World species, food-related calls are emitted by spider monkeys (Ateles geoffrey)
[Chapman & Lefebvre, 1990], different species of capuchins [Izawa, 1979;
Robinson, 1982; Boinski & Campbell, 1996], and different species of Callitrichidae, such as cotton-top tamarins (Saguinus oedipus) [Cleveland & Snowdon,
1982], pygmy marmosets (Cebuella pygmaea) [Pola & Snowdon, 1975], and
golden-lion tamarins (Leontopithecus rosalia) [McLanahan & Green, 1978; Benz,
1993].
The frequency of food calls can be influenced by different variables, including
the quantity of the food discovered [Dittus, 1984; Hauser et al., 1993], its quality
[Elowson et al., 1991; Benz, 1993; Roush & Snowdon, 2000], and its location
[Dittus, 1984]. However, relatively little information is available on the effects
that social context can have on the emission of food calls, that is, the ‘‘audience
effect.’’ This effect is observed when the absence or presence of an audience
influences the number of calls produced by an individual. The specificity of such
an effect depends, we believe, on the ecology and natural history of that particular
species. The data have been obtained mostly in birds, in which it has been
observed that the production of calls by male chickens is enhanced by the
presence of hens [Marler et al., 1986]. In the primatological literature, Caine and
collaborators have observed that red-bellied tamarins (Saguinus labiatus), when
discovering food, and when temporarily isolated from the rest of the group,
produce significantly more food calls than when in the presence of group-mates
[Caine et al., 1995]. Finally, different results have been reported for cotton-top
tamarins (Saguinus oedipus), in which different social contexts had no effect on
the production of food calls [Roush & Snowdon, 2000].
The aim of this study was to investigate whether different social contexts
influence the emission of food calls in the common marmoset. In order to better
investigate the possible effect of the social context on the quantity of food calls
produced, we decided to keep constant the characteristics of the stimulus
presented, that is, the quality and quantity of food.
METHODS
Subjects and Housing
The subjects belonged to five families of common marmoset housed at the
Istituto Superiore di Sanità in Rome. Each family was composed of a breeding
pair and their offspring of different ages (Table I), and was housed in a home cage
(220 150 80 cm) furnished with wooden perches, small trunks and branches of
different sizes, hanging objects, and a wooden nest.
The floors of the cages were covered with wood shavings. Each home cage was
connected by a system of tunnels to an experimental cage the same size as the
home cage, and located in an adjacent room. A system of sliding panels allowed
selected individuals to be sent into the experimental cage, where the tests were
performed. The rooms were kept within a temperature range of 25–281C, under a
12:12 light:dark cycle. The marmosets were fed daily with a prepared wet mix,
rich in vitamins, sugar, and dehydrated fruits, and a salad of fresh fruits and
vegetables. Hard-boiled eggs and potatoes were added weekly. Monkey pellets and
water were available ad libitum.
Food Calls in Common Marmoset / 23
TABLE 1. Composition of the Families
Breeding pairs
Family C
Cl (female; 7yrs old)
Cc (male; 7yrs old)
Cs (male; 3.5yrs old)
Cn (male; 3.5yrs old)
Ca (female; 3yrs old)
Family D
Do (female; 7yrs old)
Da (male; 6yrs old)
Dn (male; 6yrs old)
Dv (male; 6yrs old)
Family G
Go (female; 3yrs old)
Gi (male; 3.5yrs old)
Gn (female; 2.5yrs old)
Gl (male; 2.5yrs old)
Gg (male; 2.5yrs old)
Family V
Vn (female; 7yrs old)
Vl (male; 7yrs old)
Vs (male; 3.5yrs old)
Vm (female; 2yrs old)
Vi (male; 2yrs old)
Dz (female; 3.5yrs old)
Vr (male; 3yrs old)
El (female; 1.5yrs old)
Ec (female; 1yr old)
Eb (male; 1yr old)
Family VD
Procedure
We tested the breeding pair of each of the five families. We tested a pair of
individuals, rather than individuals by themselves, in order to avoid experimental
situations in which animals were left alone in a cage. We set up four experimental
conditions: 1) Isolation: the experimental pair was separated in the experimental
cage, whereas the rest of their family group was in the home cage, in the adjacent
room. 2) Visual isolation: the experimental cage was divided in two sections by a
wooden vertical panel, and the experimental pair was in the left section, whereas
the rest of its family group was in the right section of the cage, without food. 3)
Visual contact: identical to the visual isolation condition, with the exception that
the wooden panel was replaced by a wire mesh-through which the animals could
see each other without the possibility of interacting physically. 4) Physical
interaction: the vertical panel was removed and the experimental pair could
interact with the family members that had access to the food. The marmosets
were not fed in the morning before testing. In each condition the individuals were
placed in the cages 5 min before testing, and then as soon as the food was
available we started collecting the data. The food consisted of 50 g of soft cheese, a
highly preferred food [Vitale & Queyras, 1997].
Vocalization
In Callithrix jacchus, food calls are vocalizations that are uttered in the
presence of preferred foods. These calls are short, loud, chirping sounds, which
are heard only when an individual sees, manipulates, and/or eats a preferred food.
We have not heard such vocalization in other contexts, such as in the presence of
nonpreferred food or upon the discovery of new objects.
A sonogram of a common marmoset food call is presented in Figure 1.
Data Collection
The sessions for each of the four conditions lasted 15 min, divided into 90
intervals of 10 sec each. Each pair was tested twice in each experimental condition
24 / Vitale et al.
Fig. 1. Sonogram of a common marmoset food call.
(two replications), and the order of the different conditions was randomized, with
1 week between each session.
In each interval of 10 sec, and for each member of the pair, we recorded with
the one/zero sampling method the occurrence of eating (the monkey chews and
swallows the soft cheese), and the occurrence of food calls. The food calls were
identified by ear. Tests were carried out between 1000 and 1200 hr by M.Z.
Statistical Analysis
For each individual, the number of intervals in which the animal was eating
(indicated as E), and the number of intervals in which the animal was emitting
food calls while eating (indicated as Fe) were collected. In order to standardize the
data, taking into account the different number of intervals in which each animal
was eating, and depending also on the amount of food available per animal in the
different experimental conditions, the proportion of eating intervals in which food
calls were emitted (Pe ¼ (Fe/E)) was calculated. Three response variables were
then analyzed: 1) the number of eating intervals (E), 2) the number of intervals in
which food calls were emitted (Fe), and 3) the percentage of intervals in which
food calls were emitted (Pe).
To verify whether the variability among the five pairs was significantly
different from the variability between members within pairs, a parametric
analysis of variance (ANOVA) was applied to the original data (E and Fe) or
appropriately transformed data (arcsin OPe), considering pairs and animals
nested within pairs as random blocking factors, and conditions and replications as
fixed factors within animals. The test did not reveal any significant statistical
differences for pairs and replications. Consequently, pairs were not considered,
and the following statistical analyses were performed on a mean value for
individuals across replications.
The Friedman ANOVA was applied to the number of eating intervals (E), the
number of intervals in which food calls were emitted (Fe), and the proportion of
intervals in which food calls were emitted (Pe), considering the individuals as
blocks and the experimental conditions as repeated measures for each individual
[Marascuilo & McSweeney, 1977]. Multiple comparisons were performed by the
Wilcoxon test, with Bonferroni’s correction.
Food Calls in Common Marmoset / 25
RESULTS
The results show that the number of eating intervals significantly differed
among conditions (w23 ¼ 14.79, P ¼ 0.0020). In particular, conditions were graded
from ‘‘isolation’’ (lower level) to ‘‘visual contact,’’ ‘‘physical interaction,’’ and
‘‘visual isolation’’ (higher level) (Fig. 2). Multiple comparisons revealed that the
number of eating intervals was significantly lower in the ‘‘isolation’’ condition
than in the ‘‘physical interaction’’ and ‘‘visual isolation’’ conditions, and in the
‘‘visual contact’’ condition than in the ‘‘visual isolation’’ condition. Moreover,
when considering the number of intervals in which food calls occurred, a
significant difference among conditions was also found (w23 ¼ 27.48, Po0.0001).
Conditions were graded from ‘‘physical interaction’’ (lower level), to ‘‘visual
contact,’’ ‘‘isolation,’’ and ‘‘visual isolation’’ (higher level) (Fig. 2). Multiple
comparisons pointed out significant differences between all pairs of conditions,
except the ‘‘visual contact’’ and ‘‘isolation’’ conditions.
Finally, the proportion of intervals in which food calls were emitted was
different in the different conditions (w23 ¼ 28.92, Po0.0001). Specifically, conditions were graded from ‘‘physical interaction’’ (lower level), to ‘‘visual contact,’’
‘‘isolation,’’ and ‘‘visual isolation’’ (higher level). Multiple comparisons pointed
out significant differences between all pairs of conditions (Fig. 3).
Mean number of intervals
60
40
20
0
Isolation
Visual
isolation
Visual
contact
Physical
interaction
Experimental conditions
Fig. 2. Mean numbers of eating intervals (’) and mean numbers of intervals in which food calls
were emitted during eating (&) in the four different experimental conditions. Error bars are the SD
computed over the 10 animals, averaging over replications the two responses for each animal.
Mean %intervals with emission of food calls
26 / Vitale et al.
120
80
40
0
Isolation
Visual
isolation
Visual
contact
Physical
interaction
Experimental conditions
Fig. 3. Mean percentages of intervals in which food calls were emitted during eating (on the total of
intervals in which individuals were observed eating) in the four different experimental conditions.
Error bars are the SD computed over the 10 animals, averaging over replications the two responses
for each animal.
DISCUSSION
The aim of the present study was to investigate the influence of different
social contexts on the emission of food calls by common marmosets, keeping
constant the quality and quantity of food, to avoid the confounding effects of these
variables.
The results show that the proportion of intervals in which food calls were
produced by the experimental subjects increased significantly with the decrease of
the degree of social input, with the highest values recorded during the conditions
of isolation and visual isolation. Our results suggest that food calling in common
marmoset can be influenced by different social contexts.
The present findings can be discussed taking into account the state of arousal
of the caller, the possible information conveyed by food calls, and the possible
adaptive functions for the caller. Food calls can be an indication of the emotional
state of the caller (‘‘affective’’ interpretation), and/or can offer ecologically
relevant information to the potential listener (‘‘representational’’ interpretation)
[Benz, 1993]. These two interpretations are not mutually exclusive, and can
coexist in the interpretation of our results.
It has been shown that food calls are emitted by common marmosets only in
the presence of a preferred food [Queyras et al., 2000]; therefore, we suggest that,
in this species, these calls are the result of a state of arousal, as indicated in the
studies on chickens by Evans and Marler [1994]. However, since their emission
increased with the decrease in availability of family members, we hypothesize
that these vocalizations could have also the function of attracting family members
toward the preferred food source (representational hypothesis). Therefore, we can
Food Calls in Common Marmoset / 27
argue that both of these elements (affective and representational) are found in
the food calls emitted by common marmosets.
It should be noted that our findings are in contrast with those found by
Marler et al. [1986] in chickens. In that study, males were observed to call more
frequently in the presence of females than in their absence, which was
interpreted as a reproductive strategy of the males (they were silent when there
was another male around). The case of the common marmoset is different. In fact,
for this small monkey to find itself alone can be a cause of distress: their vocal
repertoire is characterized by a series of contact calls, whose function is to keep
family members close when they are temporarily out of vision. To attract family
members to a source of preferred food can be an advantage and a disadvantage at
the same time. The level of competition over food increases, but the caller can
exploit the benefits derived from living in groups, such as an increased level of
vigilance against predators, as suggested in the case of red-bellied tamarins
[Caine et al., 1995]. Different factors indicate that this could well be the case for
the common marmoset. Similar to the tamarins, Callithrix jacchus is a species of
small dimensions (average weight 350 g); it gives alarm calls against a number of
potential aerial and terrestrial predators, and the individuals move rapidly along
tree branches and can often find themselves visually isolated from the rest of the
family [Pook, 1978; Goldizen, 1987].
In conclusion, our data suggest that food calls in the common marmoset,
besides being a sign of arousal in the caller upon the discovery of a source of
preferred food, could have a communicative function as well, in transmitting
information about the location of palatable food to family members. Furthermore,
these calls could represent an advantage for the caller, because by attracting
nearby family members the caller can increase the general level of antipredator
vigilance.
ACKNOWLEDGMENTS
We acknowledge Nancy Caine and Marco Bologna for their suggestions and
advice at different stages of the study. Furthermore, we acknowledge Gemma
Calamandrei, Elisabetta Visalberghi, and Elsa Addessi for their critical reading of
an early version of the manuscript. Finally, we thank Emanuele Licata for
providing the sonogram of a food call.
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