Degree of social contact affects the emission of food calls in the common marmoset (Callithrix jacchus).код для вставкиСкачать
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: firstname.lastname@example.org 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 . 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.  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. REFERENCES Benz JJ. 1993. Food-elicited vocalizations in golden lion tamarins: design features for representational communication. Anim Behav 45:443–455. Boinski S, Campbell AF. 1996. The huh vocalization of white-faced capuchins: a spacing call disguised as a food call? Ethology 102:826–840. Caine NG, Addington RL, Windfelder TL. 1995. Factors affecting the rates of food calls given by red-bellied tamarins. Anim Behav 50:53–60. Chapman CA, Lefebvre L. 1990. Manipulating foraging group size: spider monkey food calls at fruiting trees. Anim Behav 39: 891–896. Cleveland J, Snowdon CT. 1982. The complex vocal repertoire of the adult cotton-top tamarin (Saguinus oedipus). Zeitschr Tierpsychol 58:231–270. Dittus WPJ. 1984. Toque macaque food calls: semantic communication concerning food distribution in the environment. Anim Behav 32:470–477. Elowson AM, Tannenbaum PL, Snowdon CT. 1991. Food associated calls correlate with food preferences in cotton-top tamarins. Anim Behav 42:931–937. Evans CS, Marler P. 1994. Food calling and audience effects in male chickens, Gallus gallus: their relationship to food availability, courtship and social facilitation. Anim Behav 47:1159–1170. 28 / Vitale et al. Goldizen AW. 1987. Tamarins and marmosets: communal care of offspring. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 34–43. Hauser MD, Teixidor P, Field L, Flaherty R. 1993. Food-elicited calls in chimpanzees: effects of food quantity and divisibility. Anim Behav 45:817–819. Izawa K. 1979. Foods and feeding behavior of wild black-capped capuchin (Cebus apella). Primates 20:57–76. Marascuilo LA, McSweeney M. 1977. Nonparametric and distribution-free methods for the social sciences. Monterey: Brooks/ Cole Publishing Company. 556 p. Marler P, Dufty A, Pickert R. 1986. Vocal communication in the domestic chicken. II. Is a sender sensitive to the presence and nature of a receiver? Anim Behav 34:194–198. McLanahan EB, Green KM. 1978. The vocal repertoire and analysis of the contexts of vocalizations in Leontopithecus rosalia. In: Kleiman DG, editor. The biology and conservation of the Callitrichidae. Washington, DC: Smithsonian Press. p 251–269. Pola YV, Snowdon CT. 1975. The vocalizations of pygmy marmosets (Cebuella pygmae). Anim Behav 23:826–842. Pook AG. 1978. The vocal response of Saguinus fuscicollis and Callithrix jacchus to pictorial stimuli. In: Chivers DJ, Herbert J, editors. Recent advances in primatology. Vol. I. Behaviour. London: Academic Press. p 835–836. Queyras A, Scolavino M, Puopolo M, Vitale A. 2000. Social influence on induced food preference in common marmosets (Callithrix jacchus). Folia Primatol 71: 367–374. Robinson JG. 1982. Vocal systems regulating within-group spacing. In: Snowdon CT, Brown CH, Peterson M, editors. Primate communication. Cambridge: Cambridge University Press. p 94–116. Roush RS, Snowdon CT. 2000. Quality, quantity, distribution and audience effects on food calling in cotton-top tamarins. Ethology 106:673–690. Vitale A, Queyras A. 1997. The response to novel foods in common marmoset (Callithrix jacchus): the effects of different social contexts. Ethology 103:395–403.