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Ethology of Friendship Among Adult Male Bonnet Macaques, Macaca radiata, at Arunachala Hill, India

Atham intro

For the past many years, as far back as I can remember, I have had the privilege of visiting a special place almost every year. The special place is Sri Ramanasramam, a spiritual retreat at the foothills of the Arunachala Mountain in Tiruvannamalai, Tamil Nadu, in southern India. This retreat is home to me. I looked forward to these visits for many reasons, but what draws me most is my growing captivation with the bonnet macaques (Macaca radiata) that inhabit the retreat and the surroundings. Year after year, I have followed, played, observed, and fed these monkey friends. I have learned so much by watching and interacting with the macaques. This last summer, for two months, I conducted a behavioral observational study on the social behavior of the adult male macaques.

Family of Macaques on roof

Family of Macaques on roof


Mammalian males commonly do not associate in affiliative and cooperative relationships. Bonnet macaques (Macaca radiata) are one of the most social primates. Unlike other mammalian males, adult males in this species frequently sit together, groom, huddle, greet, and support one another (Devore 1965, Sinha 2001, Silk 1994, Van Hooff 1994).

Background

In this section I would like to discuss the literature relating to friendship among nonhuman primates. In friendship, both emotional and material support is exchanged. These altruistic behaviors can be costly to the actor and beneficial to the recipient. There seems to be a difference in understanding between biologists and social scientists on the concept of friendship and cooperation (Silk 2003, Massen 2006). Most biologists conceive of friends as social tools to achieve fitness-related benefits (Massen 2006). Models for social relationships revolve around tit-for-tat reciprocal altruism. In contrast, most social scientists' definitions of friendship stress concern for each other's well-being and a willingness to help each other without expecting repayment (Massen 2006 ). The social science literature suggests that tit-for-tat reciprocity is characteristic of relationships among casual acquaintances and strangers, not among friends. Human primates value balanced reciprocity in their relationships with friends but avoid keeping careful count of the benefits given and received, and are offended when friends reciprocate immediately and directly (Silk 2003).

The purpose of this study is to address the question whether adult male bonnet macaques enjoy friendship. I addressed the question by closely investigating the social structure among bonnet macaque adult males. The objectives of the study are to examine:

  • Do affiliative relationships exist between adult male bonnet macaque dyads?
  • Does the strength of the social/affiliative relationships vary among dyads?
  • Is there time-matched reciprocity in social relationships among dyads? If so, find the level of reciprocity within a bout of grooming, or within a short span of time (such as a day), or if there is overall reciprocity.
  • Is there a correlation between the strength of affiliative relationships and dominance ranks among adult males?

Answers to these questions will help address whether adult male bonnet macaques enjoy friendship among other males in the group. Based on my preliminary observations, I hypothesized that the adult males enjoy social relationships with other males within the group, and that there is some level of reciprocity of affiliative behavior among dyads.

Methods and Materials

I used seven bonnet macaque adult males belonging to one group as subjects of this study. The group consists of multiple male and female adults, with several juveniles and infants. The independent variables are the individual adult male macaques; the dependent variables are the duration and frequency of affiliative activity; and the constants are the same species, the same group of macaques, and the same location.

I conducted the study by first identifying the individual macaques, then determining the dominance hierarchy within the adult males of the group, and then using focal sampling to gather data on affiliative behavior between the adult males. At the study site I carefully observed the adult males and identified the individuals by recording distinct marks (e.g. scars, length of tail, marks on face or body). I ignored the females, the juveniles, and infants in the group.

I created a dominance hierarchy matrix of the adult males in the group by observing incidents with dominant gestures. The most common dominant gestures were: one macaque approaches another and the other avoids him or leaves; or one macaque supplants another at a desirable resource such as food or a grooming partner. The other dominant gestures observed were: stare threatening, eyelid threatening, open-mouth threatening, and growl threatening (Devor 1965). The ranking of the macaques was most evident when a single portion of food was placed between the two males. The higher ranked macaque would consistently take the food.  

Two adult male Macaques

Two adult male Macaques


I conducted focal sampling of the individual adult males in the group throughout the day. The focal samples were each 15 minutes long. Within each focal sample, I recorded occurrences of all behavior of the focal male (Altmann 1974). I also recorded the duration of the specified behavior. If the behavior involved another macaque, I also recorded this associated macaque. I conducted more than 150 hours of focal sampling, resulting in 600 focal samples of 15 minutes each. I then analyzed the data gathered from the focal sampling of the adult males.

Sociality index
For the sociality index, I determined the strength of the social relationship within the dyads based on the frequency and duration of time spent in affiliative activities within the dyad. I considered grooming and being in proximity as affiliative activities. I established an index of sociality as a composite of grooming and being in proximity (sitting, eating, resting, and playing close to each other).

I defined the strength of a social relationship based on duration as

(Duration of time spent together grooming and being in proximity)
 (Total sample time of both dyad members)

Based on the frequency of occurrence of affiliative behavior, the sociality index is defined as

NAB  /  (NA + NB + NAB ), where NAB = no. of occasions A and B are seen together; NA = no. of occasions A is seen without B; and NB = no. of occasions B is seen without A (Martin 1986).

Reciprocity index

Reciprocity index


I used the reciprocity index to measure the quality of social bonds (see equation at right). The reciprocity index represents the reciprocity of grooming in a dyad (Chancellor 2008). Information about grooming given and received was used to measure how evenly the grooming was balanced within dyads. The absolute difference between the proportion of the pair's grooming that was performed by each partner, a score that will be 0 for a completely equitable relationship and 1 for a relationship that is maintained completely by one of the partners. This value was subtracted from 1 so that the "grooming index" would be greatest, 1, when the relationship was most equitable; and 0 when it was least equitable (Silk 2006). I compared the sociality indices of the dyads with the reciprocity index to see if there was reciprocity within a social relationship.

Dominance-affiliative distance
For each affiliative relationship, I computed the difference in dominance ranks between the members of the dyad, and compared with the strength of affiliative relationship. This way I determined the dominance ranking and affiliative distance. I used the answers to the above questions to address if adult male bonnet macaques exhibit friendship.

Results

Identification of Individuals
The subjects for my study comprised of seven adult male bonnet macaques belonging to the same group that visited the grounds of Sri Ramanasramam. Table 1 presents the seven individuals with their distinct features. I gave the macaques names inspired by the characters in The Chronicles of Narnia, though there was little similarity in personality between the characters and the macaques.

Table 1: Identification of Individuals

Table 1: Identification of Individuals


Table 2: Dominance Hierarchy of Adult Males (Most Dominant Animal is Top Left)

Table 2: Dominance Hierarchy of Adult Males (Most Dominant Animal is Top Left)


Figure 1: Strengths of Social Relationships: Varies Among Dyads In this essay a dyad is a pair of monkeys, represented by two letters, each being the first letter of the name given to a monkey. So the dyad "O-P" represents the pair of macaques "Otmin" and "Peter". "O-P" and "P-O" represent the same pair of macaques.)

Figure 1: Strengths of Social Relationships: Varies Among Dyads In this essay a dyad is a pair of monkeys, represented by two letters, each being the first letter of the name given to a monkey. So the dyad "O-P" represents the pair of macaques "Otmin" and "Peter". "O-P" and "P-O" represent the same pair of macaques.)


Table 3: Sociality Index created based on duration

Table 3: Sociality Index created based on duration


Figure 2: Sociality index created based on duration of affiliative behavior within dyads

Figure 2: Sociality index created based on duration of affiliative behavior within dyads


Figure 3: Sociality index based on frequency and order of social relationships

Figure 3: Sociality index based on frequency and order of social relationships


Table 4: Sociality Index Based on Frequency

Table 4: Sociality Index Based on Frequency


Figure 4: Correlation Between Sociality Indices Based on Duration and Frequency

Figure 4: Correlation Between Sociality Indices Based on Duration and Frequency


Table 5: Comparison between Sociality Index based on duration and frequency

Table 5: Comparison between Sociality Index based on duration and frequency


Figure 5: Reciprocity Index within a Bout

Figure 5: Reciprocity Index within a Bout


Figure 6: Reciprocity Index within a Day

Figure 6: Reciprocity Index within a Day


Table 7: Reciprocity Index within a Day

Table 7: Reciprocity Index within a Day


Figure 7: Reciprocity Index within Sampling Period of Two Months

Figure 7: Reciprocity Index within Sampling Period of Two Months


Table 8: Reciprocity Index within Sampling Period of Two Months

Table 8: Reciprocity Index within Sampling Period of Two Months


Figure 8: Correlation Between Sociality Indices (Duration and Frequency) and the Reciprocity Index

Figure 8: Correlation Between Sociality Indices (Duration and Frequency) and the Reciprocity Index


Table 9: Comparison Between Dominance Ranking Distance and Strength of Reciprocity

Table 9: Comparison Between Dominance Ranking Distance and Strength of Reciprocity


Figure 9: Comparison Between Dominance Ranking Distance and Sociality Index Based on Duration

Figure 9: Comparison Between Dominance Ranking Distance and Sociality Index Based on Duration


Figure 10: Comparison Between Dominance Ranking Distance and Sociality Index Based on Frequency

Figure 10: Comparison Between Dominance Ranking Distance and Sociality Index Based on Frequency


Dominance Hierarchy
I determined the dominance hierarchy of the seven adult males by observing them for dominance gestures, as well as ranking them based on food seizing. Table 2 presents the dominance hierarchy of the adult males. The numbers indicate the total number of incidents in which the monkey in the first column acted in a dominant manner toward the monkey in the righthand column during a two-month period.  

Sociality Index
I created the sociality Index of the adult male macaques by analyzing the duration and frequency of affiliative behavior between the dyads. Macaques with higher sociality index scores have stronger social bonds.

I created the sociality index based on the duration of affiliative behavior for the various social relationships, as shown in Figure 1. Figure 1 (and Table 3) shows that an adult male macaque can enjoy varying degrees of social relationships with other adult males. The strength of the social relationships varied among the dyads. From Figure 2, we can see that a ranking exists for the strengths of social relationships between the various dyad members in a group.

I created a sociality index based on frequency as shown in Figure 3. From Figure 3 and Table 4, we can see that strengths of social relationships in dyads, based on frequency, can be ranked or ordered in a group. Figure 4 (and Table 5) show a positive correlation of 0.87 between the sociality indices determined based on the duration and based on frequency of affiliative behavior between the dyad members.

Reciprocity Index
 I used the reciprocity index to assess the quality of the various social relationships. From Figure 5 (and Table 6), we can see that the adult male macaques rarely (i.e. in 3 out of 20 dyads) reciprocated grooming within a bout of grooming. Reciprocity within a day (from Figure 6 and Table 7) increased when compared to reciprocity within a bout, with 10 out of 20 dyads participating in reciprocity. But the levels of reciprocity were 0.3 or less, showing that the reciprocity was not nearly equal. Reciprocity within the sampling period of two months (Figure 7 and Table 8) shows that nearly all dyads participated in reciprocity, but the levels of reciprocity varied among the dyads from 0.8 (closer to equal reciprocity of 1) to less than 0.1.

Figure 8 (and Table 9) show a positive correlation of 0.89 between the sociality index based on duration and the reciprocity index. The correlation between the sociality index based on frequency and the reciprocity index was 0.85.

Figures 9 and 10 show the comparison of dominance ranking distance and sociality index based on duration and frequency, respectively. Figure 9 shows a negative correlation of 0.85 between dominance ranking distance and sociality index based on duration within dyads. Figure 10 shows a negative correlation of 0.93 between dominance ranking distance and sociality index based on frequency within dyads.

Discussion

In this study, I conducted a close investigation of the social structure of the adult male bonnet macaques. I identified the seven individual adult males through distinct traits and given names. I observed the subjects for dominant gestures. I recorded a dominance hierarchy of the adult males within the group. I created sociality indices by ordering the strengths of social relationships based upon the frequency and duration of affiliative behavior within the dyads. I obtained a distinct ordering of social strengths of relationships within the dyads. Also, the strength of social relationship varied among the dyads. These observations lead me to believe that the adult male macaques enjoy social relationships with other males, and they define a unique social structure within each group. The two sociality indices, based on the duration and frequency of social relationships, had a positive correlation, thus allowing either index to represent the strength of social relationships among the males in the group. This could be valid for adult males, who are not as restless as juveniles or sub-adults. Typically it was observed that when a grooming bout was initiated, the grooming tended to last for a significant time. Hence the correlation between sociality indices based on frequency and duration of affiliative behavior seems valid for adult males.  

I determined the quality of social relationships by computing the reciprocity index. There was virtually no or low reciprocity of grooming within a bout of grooming within the dyads. Within a day, however, there was some level of reciprocity of grooming. Over the sampling period of two months, there was significant amount of reciprocity within the dyads. This indicates that adult male bonnet macaques tend not to indulge in immediate tit-for-tat reciprocity in affiliative behavior; they do not immediately pay back grooming favors. However, over a longer period of time, the stronger social relationships showed higher levels of reciprocity. This behavior trend is more along the lines of the social scientists' perception of friendship, where there is overall concern and care for each other, but active immediate accounting is not maintained to track the amount of grooming given or received.

For the various dyads, we saw that there was negative correlation between dominance ranking distance and the sociality indices. This shows that the most dominant male macaques do not enjoy reciprocal affiliative relationships with the lowest ranking males.

Conclusion

The study provided an insight into the social structure of the adult male bonnet macaques at Arunachala Hill. Unique to bonnet macaque species, the adult males do enjoy affiliative relationships with other males in the group. The males enjoyed varying strengths of social bonds with other males. There was little reciprocity of grooming within a bout or within a short period of time such as a day. This demonstrated that the males did not indulge in tit-for-tat reciprocity. However, the males demonstrated reciprocity in grooming over the sampling period of two months. The stronger social relationships also demonstrated higher levels of reciprocity. The social behavior of the males leaned more towards the social scientists' definition of friendship, with overall concern and care for each other.

I would like to continue work to confirm the findings from this study by conducting focal sampling of adult male macaques belonging to more than one group, in different locations, and also by extending the sampling period, to see if friendship is demonstrated over even longer periods of time.

The findings from this study support that adult male bonnet macaques enjoy friendship, which leads us one step further to the mystery of whether friendship is an evolutionary characteristic passed on from nonhuman primates to humans.

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