Journal of Comparative Psychology 2008, Vol. 122, No. 1, 94 –99
Copyright 2008 by the American Psychological Association 0735-7036/08/$12.00 DOI: 10.1037/0735-7036.122.1.94
An Experimental Investigation of Referential Looking in Free-Ranging Barbary Macaques (Macaca sylvanus) Sam G. B. Roberts and Karen McComb
Ted Ruffman
University of Sussex
University of Sussex and University of Otago
The authors examined looking behavior between 15 Barbary macaque (Macaca sylvanus) infants and their mothers in the presence of a rubber snake (experimental period) and in the absence of the snake (control period). Two of the 15 infants looked referentially at their mother in the experimental period. Including both referential and nonreferential looks, the six older infants (aged 5 to 12 months) displayed a higher frequency of looks to mother than nine younger infants (aged 3 to 4.5 months) in the experimental period, but not in the control period. Older infants looked more to the mother in the experimental condition, whereas the younger infants looked more to the mother in the control condition, or looked equally in the two conditions. These results suggest that age is an important factor in determining looking behavior to mother in situations of uncertainty. Compared to hand-reared chimpanzees or human infants tested in standard social referencing paradigms, the infant macaques displayed a low rate of referential looking. Possible explanations for this are discussed. Keywords: social referencing, Barbary macaques, referential looking, nonhuman primates
clear adaptive value, especially in relation to biologically relevant stimuli like snakes. If an infant can somehow “tap into” the knowledge possessed by its conspecifics, and in particular its mother, it can avoid making costly errors associated with individual trial-and-error learning (Russell et al., 1997). Russell et al. (1997) found good evidence of social referencing between hand-reared chimpanzees and their human caregivers. When exposed to a novel object, the chimpanzees looked referentially at their human caregivers and adjusted their behavior according to whether they received a “happy” or “fear” message from the caregiver. However, two studies of captive mother-infant pairs of chimpanzees (Itakura, 1995; Tomonaga et al., 2004) found no evidence of referential looking between the infant and mother, and only limited evidence of behavioral regulation based on the emotional information received from the mother. From these results, it is unclear whether the referential looking obtained by Russell et al. (1997) is a product of enculturation, or whether conspecific mother-infant pairs would also show referential looking if tested in a different experimental paradigm. The importance of making comparisons between different species—and taxa— of primates in furthering our understanding of the phylogenetic origins of specific cognitive abilities is widely acknowledged (Suddendorf & Whiten, 2001). Referential looking in situations of uncertainty is present in human infants and handreared chimpanzees—the current study examines whether this process of referential looking is also present in a monkey species, the Barbary macaque. Macaque infants were exposed to a rubber snake while mothers were nearby and infant reactions were recorded. If Barbary macaques seek information from their mothers in situations of uncertainty, we predicted that infants would show a higher frequency of looks and physical contact with the mother in the experimental period compared to the control period, as they sought information from the mother about the appropriate response to the snake. Specifically, we predicted that infants would look
Social referencing is defined as the seeking of information from another individual and the subsequent use of that information to evaluate an object or event (Sorce, Emde, Campos, & Klinnert, 1985). There are two components to social referencing: referential looks alternating between another individual and the object or event, and behavioral regulation based on the emotional information received (Russell, Bard, & Adamson, 1997). Social referencing occurs from around 12 months in human infants (Sorce et al., 1985; Walden & Baxter, 1989) and enables an individual to learn the meanings of objects and social interactions they have not personally experienced. In nonhuman primates, this would have
Sam G. B. Roberts, Department of Psychology, University of Sussex; Karen McComb, Department of Psychology, University of Sussex; and Ted Ruffman, Department of Psychology, University of Sussex and University of Otago. Sam Roberts is now at the Institute of Cognitive and Evolutionary Anthropology, University of Oxford. This work was funded by a Biotechnology and Biological Sciences Research Council Special Studentship to S. R. under the supervision of K. M. and T. R. This article is based on part of a doctoral dissertation submitted by Sam G. B. Roberts to the University of Sussex. Dr. John Cortes and Eric Shaw of the Gibraltar Ornithological and Natural History Society provided invaluable assistance to enable the experiments in Gibraltar to be completed. The staff at Gibraltar Transmitter and Aerials Sections provided access to the Middle Hill site. Dr. Stuart Semple introduced S.R. to the Barbary macaques and provided invaluable advice on conducting the experiments. Tanya Lee assisted with the reliability scoring. Correspondence concerning this article should be addressed to Sam Roberts, Institute of Cognitive & Evolutionary Anthropology, University of Oxford, 58A Banbury Road, Oxford OX2 6QS, United Kingdom. E-mail:
[email protected] 94
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referentially to their mothers in the presence of the snake. Referential looks were defined as looks to the mother that were immediately (within 2 s) preceded and/or followed by a look to the novel object (following Russell et al., 1997). Referential looks demonstrate the infant is seeking information specifically about the referent, rather than looking to the mother for other reasons such as reassurance (Clyman, Emde, Kempe, & Harmon, 1986). This distinction is important in determining if the infant actively seeks out information in situations of uncertainty, or passively consumes information (Baldwin & Moses, 1996). In both human infants (Walden & Baxter, 1989) and hand-reared chimpanzees (Russell et al., 1997), older infants look more at mothers or caregivers than younger infants in situations of uncertainty. Therefore, we also compared looking behavior in younger and older macaque infants. The methodology used in our study potentially provides a powerful technique that allows for referential looking in infants to be explored experimentally in free-ranging nonhuman primates. Previous studies examining referential looking in infants have used captive chimpanzees (Itakura, 1995; Russell et al., 1997; Tomonaga et al., 2004). There have been reports of free-ranging macaques looking at other conspecifics in response to the presentation of snake models, leopard models, or the playback of alarm calls (Coss & Ramakrishnan, 2000; Ramakrishnan, Coss, Schank, Dharawat, & Kim, 2005; see also: Seyfarth & Cheney, 1986) and these studies found that individuals display flight behavior after monitoring the behavior of conspecifics fleeing a perceived threat, demonstrating the importance of social monitoring in antipredator behavior. However, because infants spend a large proportion of their time in contact with the mother, these studies were restricted to focusing on the looks of juveniles and subadults toward conspecifics. Moreover, they did not specifically examine referential looking or other looks specifically between infants and mothers. The stimulus used to elicit referential looking in this study was a rubber snake. Catarrhine primates have had continuous coexistence with venomous snakes throughout their evolutionary history (Isbell, 2006), and primates’ response to snakes has been extensively studied, both in captivity (Mineka, Davidson, Cook, & Keir, 1984) and in the wild (Ramakrishnan et al., 2005). Fear of snakes in primates is widespread throughout the primate order (Ohman & Mineka, 2003). The development of fear of snakes in primates appears to involve both an innate tendency to exhibit behavioral inhibition in the presence of snakes (Nelson, Shelton, & Kalin, 2003) and an observational learning component which leads to a strong and persistent fear of snakes (Mineka et al., 1984). Lesion studies have shown that both the amygdala (Amaral, 2002; Prather et al., 2001) and the orbitalfrontal cortex (Izquierdo, Suda, & Murray, 2005) are involved in the fear response to snakes, which is present in rhesus macaque infants at 8.5 months (Prather et al., 2001). Prior to the emergence of fear of snakes, primate infants have been observed to approach and investigate snakes (Ramakrishnan et al., 2005). The aim of the present study was to create a situation in which infants may look to their mother in response to a potential threat, rather than to explore infants’ responses to snakes per se, or to reproduce any specific threat the macaque infants may have faced from snakes in Gibraltar. The first written record of the Barbary macaques on Gibraltar dates from 1704 (Fa, 1991), and the most probable source of the extant Gibraltar colony are macaque populations in both Morocco and Algeria (Modolo, Salzburger, &
Martin, 2005). There are seven different species of snake present in Gibraltar: the horseshoe whip snake (Coluber hippocrepis), the southern smooth snake (Coronella girondica), the ladder snake (Elaphe scalaris), the montpellier snake (Malpolon monspessulanus), the false smooth snake (Macroprotodon cucullatus), the viperine snake (Natrix maura) and the grass snake (Natrix natrix; Cortes, 1982). The snakes found on Gibraltar are unlikely to pose a threat to infant Barbary macaques—none of the snakes are venomous and the constrictors are too small to endanger infant macaques. However, Barbary macaques give an alarm call to snakes, respond to playbacks of snake alarm calls with a startle response, and upon seeing a snake sometimes stand bipedally and peer into the grass around them, or approach and mob the snake (Fischer & Hammerschmidt, 2001). Snakes thus appear to be a highly salient, biologically relevant stimulus for Barbary macaques.
Method Subjects The experiments were carried out on free-ranging Barbary macaques (Macaca sylvanus) in Gibraltar, a limestone outcrop at the southern end of the Iberian peninsula, which is 5 km long and just over 1 km wide. All macaque adults used in the study over 3 years of age were individually recognized using a combination of facial markings and tattooed identification numbers. All macaques were fully habituated to humans. The age of the infants was determined by personal observation of the arrival of new infants, within two days of the birth. For analysis, the infants were split into two groups—nine younger infants aged 3 to 4.5 months (M ! 3.89 months, 95% confidence interval [CI] ! 3.57 and 4.21) and six older infants aged 5 to 12 months (M ! 8.75 months, 95% CI ! 5.00 and 12.50).
Procedure A green and black rubber toy snake measuring 100 cm in length and 9.8 cm in diameter at its thickest point was used as the stimulus. Mother-infant pairs were identified based on individual recognition of the mother and suckling by the infant. When the mother-infant pair was seated and engaged either in suckling, grooming or resting, the snake was placed nearby (1 to 20 m away), but not directly in their line of sight (see Figure 1). During the placement of the snake, care was taken to ensure that the mother and infant were facing away and thus did not observe the snake. The response of the infant when they came across the snake was videotaped, using a Sony CCD-TR550E 8 mm video camera. Video recording continued until the mother and infant left the area, or there was a risk that other macaques would see the snake. At the end of both the successful and unsuccessful trials, the snake was concealed with a bag and then removed. None of the infants had seen the snake before encountering it in the experimental trial. In all the trials included in this study, the infant saw the snake before the mother. Each experimental trial was paired with a matched control period where the same mother-infant pair was present. This period of monitoring was selected to be as close as possible in time to the experimental trials, so that the infants’ age was similar in the experimental and control periods. The control periods were com-
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Figure 1. Photo of experimental set up for social referencing experiment showing mother, infant and snake. The mother is lying down beside the wall and her infant is sitting up beside her. The snake is on the other side of the wall to the mother and infant.
posed either from the time just before the snake was seen in the experimental trials, or from aborted experimental trials when the snake had not been seen.
Behavioral Coding The infants’ behavior in the period after they first looked at the snake was classified into three mutually exclusive and exhaustive categories: (a) move closer to snake, (b) move further away from the snake, or (c) no reaction. Additionally, whether the infant touched the snake, picked up the snake or gave any vocalization was recorded. The distance at which the infant encountered the snake (less than or more than 1 m) was also recorded. The initial investigation of the snake by the infant ended when it moved out of the immediate vicinity of the snake, defined as the area in which the infant was within 2 m and had a clear line of sight to the snake. If the infant subsequently moved back into the vicinity of the snake, this was defined as a “reinvestigation.” All looks (both referential and nonreferential) by the infant to the mother while the infant was in the immediate vicinity of the snake were recorded. Nonreferential looks were defined as looks by the infant to the mother that were not immediately (within 2 s) preceded and/or followed by a look to the snake. In both the experimental and control periods, only the time the infant was out of physical contact with the mother was used to calculate the rate of looks per minute. Trial time was measured using the video time stamp. The mean time of the experimental trials was 86.47 s (95% CI ! 55.30 and 117.63), and the mean time of the control trials was 72.40 s (95% CI ! 39.00 and 105.80). In all trials, the snake was out of sight of the mother, and this study focused solely on looks by the infant to the mother. To establish reliability of the coding scheme, the primary coder coded all of the data and the second coder coded 21% of the data. In cases of disagreement, the primary coder’s decision was used. The categorical judgments on the infants’ initial reaction to the snake, and the number of reinvestigations were straightforward
and unambiguous and agreement for the portion that both coders coded was at 100% for all these categories with a Cohen’s Kappa of 1.0. For all infant looks to mother, percentage agreement was calculated by dividing the number of times the two coders agreed on the number of looks given, by the total number of looks, using the primary coder’s number of looks over the stimuli that were coded by both coders. A look could occur when the infant first saw the snake, and also each time the infant reinvestigated the snake. For the number of infant looks to the mother, the two coders were in agreement in 17 out of the 20 judgments made, giving a percentage agreement of 85%. The two coders never disagreed by more than one look on the number of looks given. Initial analysis showed that the data on the rate of looks per minute was not normally distributed, so nonparametric statistics were used in all comparisons. An alpha level of .05 was used for all statistical tests.
Results Six of the younger infants moved further away from the snake after the initial sighting, with three infants moving closer. Two of the older infants moved further away from the snake, with the other four infants moving closer. We tested for a statistically significant difference in the proportion of young and old infants displaying different initial responses to the snake using Fisher’s exact test. There was no statistically significant difference between younger and older infants’ initial response to the snake (approach/ move away), Fisher’s exact test: N ! 15, p ! .32, Cramer’s V ! 0.33. There was no relationship between whether the infant saw the snake at a distance of less than or more than 1 m, and their initial response to the snake, for either younger (Fisher’s exact test: n ! 9, p ! 1.00, V ! 0.16) or older (Fisher’s exact test: n ! 6, p ! .40, V ! 0.71) infants. None of the 15 infants tested gave an alarm call in response to seeing the snake, and only one infant (aged 5.5 months) touched the snake. Four of the younger infants, and all six of the older infants reinvestigated the snake at least once. There was no statistically significant difference in the number of rein-
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vestigations made by younger (Mdn ! 1) versus older infants (Mdn ! 3.5), Mann–Whitney U ! 14.0, n1 ! 9, n2 ! 6, p ! .13, r ! "0.40. Two of the 15 infants looked referentially at their mother in the experimental period. Both of these infants (aged 4 months and 5.5 months) looked once between the snake and the mother. The low rate of referential looking precluded any statistical analysis of these looks. We then examined rate of looks per minute between mother and infant, which encompasses all looks by the infant to the mother. While in the vicinity of the snake, the older infants had a significantly higher frequency of looks to mother than the younger infants, Mann–Whitney U ! 10.0, n1 ! 9, n2 ! 6, p ! .04, r ! "0.55. In contrast, in the control periods there was no statistically significant difference between old and young infants in the frequency of looks to mother, Mann–Whitney U ! 26.0, n1 ! 9, n2 ! 6, p ! .95, r ! "0.03 (see Table 1). There were no statistically significant differences between old and young infants in the frequency of physical contact between infants and mothers in the experimental periods, Mann–Whitney U ! 26.5, n1 ! 9, n2 ! 6, p ! 1.00, r ! "0.02, or in the control periods, Mann– Whitney U ! 18.0, n1 ! 9, n2 ! 6, p ! .31, r ! "0.28. To examine looking behavior in the experimental and control conditions in the two age categories, infants were divided into two groups: (a) infants that looked more to the mother in the experimental condition than the control condition; (b) infants that looked more to the mother in the control condition than the experimental condition, or looked equally in the two conditions. There was a significant difference between older and younger infants, Fisher’s exact test: N ! 15, p ! .01, V ! 0.72. Five of the six older infants looked more to the mother in the experimental condition (the other not looking in either condition), whereas eight of the nine younger infants looked more to the mother in the control condition or looked equally in the two conditions.
Discussion This study provides the first experimental investigation of referential looking in nonhuman primate infants in the field. The most important finding is that older macaque infants (aged 5 to 12 months) had a significantly higher frequency of looks to mother in the experimental condition than younger infants (aged 3 to 4.5 months). This difference was not present in the control condition.
This suggests that in Barbary macaque infants, as with human infants (Walden & Baxter, 1989) and enculturated chimpanzees (Russell et al., 1997), older infants look more at mothers or caregivers than younger infants in situations of uncertainty. At least two factors may lie behind the age-related difference in looks to mother. First, older infants are more likely than younger infants to have had prior exposure to snakes, or to other conspecifics reacting fearfully to snakes. Through either direct experience or through observational conditioning processes (Mineka et al., 1984), older infants may treat the rubber snake as a more dangerous stimulus than do younger infants, leading to more looking to the mother. Second, both the amygdala and orbitalfrontal cortex show postnatal development in macaque infants, with full development of the latter not occurring until the end of the first year (Machado & Bachevalier, 2003). This brain development may result in a more mature appraisal of potentially dangerous stimuli in older infants, promoting greater looking to the mother for information. There may also be an interaction between the maturing brain and the exposure to snakes (or to conspecifics reacting fearfully to snakes) in that observational learning may only be effective with a certain level of brain development, or that brain maturation would not take place without the requisite environmental experience. Captive studies, where infants’ exposure to snakes can be controlled, would be necessary to resolve how brain maturation and exposure to snakes might interact to shape infants’ reactions to snakes and tendency to look at their mothers. Two of the 15 infants (one younger infant aged 4 months, one older infant aged 5.5 months) looked referentially, each infant giving one referential look between the snake and the mother. In comparison to previous studies, a low percentage (13%) of the macaque infants displayed referential looking. All 17 hand-reared chimpanzees tested by Russell et al. (1997) looked referentially at their human caregivers, while in human studies between 69% to 100% infants display spontaneous referential looking (Baldwin & Moses, 1996). There was no evidence of referential looking in captive mother-infant pairs of chimpanzees (Toyonaka et al., 2004), although only three infants were tested. An important difference between these studies and ours is that in the standard social referencing paradigm (Sorce et al., 1985; Russell et al., 1997), the mother and infant can both see the ambiguous stimulus,
Table 1 Mean Rate of Looks and Physical Contact With Mother of Barbary Macaque Infants by Age in Presence and Absence of Snake Mean rate per min Infant behavior Snake present Looks Physical contact Snake absent Looks Physical contact
95% confidence interval
Younger infantsa
Older infantsb
Younger infants
Older infants
0.58* 0.53
2.53* 0.39
"0.24–1.36 "0.14–1.21
"0.08–5.15 "0.10–0.87
1.58 0.69
1.36 0.43
"0.28–3.43 0.27–1.10
"0.27–2.99 "0.02–0.87
Note. Looks include both referential and non-referential looks by the infant to the mother. Younger infants were 3 to 4.5 months old (n ! 9). b Older infants were 6 to 12 months old (n ! 6). * p # .05. a
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whereas in the current study, the snake was out of sight of the mother. This design was necessary to ensure that the infant was not in contact with the mother when they saw the snake. As the mother was some distance away from the snake, the macaque infants may have been less likely to look referentially between the snake and the mother than the chimpanzee and human infants. Thus, the extent to which different primate species display referential looking, and the role of enculturation in this behavior, is still poorly understood. In social referencing studies, referential looking provides a means of determining whether looks by the infant to the mother are specifically to seek information about the referent, rather than for other purposes such as reassurance (Clyman et al., 1986). An important question raised by this study, given the low number of infants that looked referentially, is whether the looks by the older infants to mother in the experimental condition are simply for reassurance, or to gain information about the snake. If the looks are primarily for reassurance, we would predict that the younger infants would look more to the mother in the presence of a novel object than older infants. However, in our study, it was the older infants not the younger ones who looked to the mother in the experimental condition. One way to adjudicate between these two possibilities in future studies would be to examine infants’ looks to other conspecifics, as well as the mother. Human infants look to the mother for attachment, but will also look to other individuals for information about novel objects (Stenberg & Hagekull, 2007). Thus, if the older infant looks are primarily for attachment/ reassurance, they should be directed exclusively at the mother, whereas if they are for information-seeking, they should also be directed at other nearby conspecifics. Looks to other conspecifics were not recorded in the present study but could be included in future studies through the use of two video cameras. The infants’ behavior toward the snake was cautious, but not fearful. Seven of the infants approached the snake, and 10 of the infants reinvestigated the snake. None of the infants exhibited a strong fear reaction to the snake, in terms of freezing, fleeing, or alarm calling. A notable feature of the young infants’ behavior in the presence of a snake was the absence of looks to mother—six of the nine younger infants did not look to the mother at all during the experimental period. There were no other noticeable behaviors that reliably occurred in the presence of the snake. In a separate study examining Barbary macaque mothers’ reactions to the same rubber snake, the mothers showed stronger avoidance after their initial sighting of the snake, with 11 of the 13 mothers tested moving further away from the snake, one showing no reaction and only one moving closer to the snake (Roberts, 2004). In the present study, we used a single snake, making it uncertain whether macaques would respond similarly to all snakes. It is possible that a different snake would not have caused looks to the mother, or alternatively, that a more marked fear response and accompanying looks to the mother would have occurred had the snake moved or had it been real. However, Mineka et al. (1984) found that wild-reared rhesus monkeys reacted fearfully both to a live snake and a stationary rubber toy snake. Further, bonnet macaques show a higher rate of looks to conspecifics in response to an ambiguous stimulus such as a nonvenomous snake or an upside down leopard model compared to an intensely fearful stimulus such as a venomous snake or an upright leopard model (Coss & Ramakrishnan, 2000; Ramakrishnan et al., 2005) A live
snake may, therefore, be less likely to elicit referential looking than the stimulus used in the current study. The present experiment has two implications for future research. First, the strength of the methodology used in this study is that it provides a relatively simple common procedure which can be used to examine referential looking in infants across a wide range of primate species in both captive animals and—importantly—in field settings. Second, our finding of age effects in infancy suggests that these should be examined in future experiments with primates, and indeed, with other animal species.
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Received May 30, 2007 Revision received December 6, 2007 Accepted December 13, 2007 !
