Macaca Fascicularis)

SOCIAL RECIPROCITY AND INTERCHANGE IN LONG-TAILED MACAQUES

(MACACA FASCICULARIS)

MICHAEL DAVID GUMERT

(Under the Direction of Irwin S. Bernstein)

ABSTRACT

Social grooming is a common and potentially valuable act for long-tailed macaques. It may be traded reciprocally or interchanged with other acts such as tolerance, sexual activity, and infant handling. Social exchange related to grooming may be contingent on specific acts of

grooming, and thus traded, or it may just be a by-product of social relationships and thus not

traded. If grooming can be traded, biological market theory predicts that grooming may be

considered as “payment” for other social acts and would vary with supply and demand of

available partners. If grooming is traded directly as payment for other social acts, specific acts of grooming should facilitate reciprocation and interchange. Also, the number of available partners

(i.e. supply) should negatively influence grooming duration. In the first study, I analyzed sequences following grooming bouts to test the hypothesis that reciprocation and interchange can be linked to specific acts of grooming. I found that specific acts of grooming facilitated subsequent reciprocation and interchange with tolerance or sexual activity. In the second study, I investigated exchange patterns of female-to-mother with infant grooming and its relation to the supply of infants. I found that after mothers with infants received grooming from a female, infant contact by the grooming female was facilitated. I also found a negative relationship between

grooming bout duration and the number of infants per female surrounding female-to-mother

grooming bouts associated with infant handling. It seemed that grooming did facilitate infant handling and that grooming duration was negatively related to infant supply. In the third study, I investigated whether there was a relationship between grooming duration and the supply of

females around male-to-female grooming bouts associated with mating. I found a negative

relationship between bout duration and the number of females per male surrounding a mating-

related grooming. From these studies, I concluded that specific acts of grooming can facilitate

reciprocation and interchange and that the supply of partners is related to the amount of

grooming payment an individual will offer to their partner. Overall, some grooming exchanges

appear to occur as trades, where grooming is “payment” for other social acts such as more

grooming, tolerance, sexual activity/mating, and infant handling.

INDEX WORDS: Macaca fascicularis, Long-tailed macaque, Grooming, Tolerance, Sex, Mating, Infant handling, Reciprocity, Interchange, Biological market theory

SOCIAL RECIPROCITY AND INTERCHANGE IN LONG-TAILED MACAQUES

(MACACA FASCICULARIS)

MICHAEL DAVID GUMERT

B.S., East Stroudsburg University, 1997

M.S., Bucknell University, 2001

A Dissertation Submitted to the Graduate Faculty of The University of Georgia in Partial

Fulfillment of the Requirements for the Degree

DOCTOR OF PHILOSOPHY

ATHENS, GEORGIA

2006

Michael David Gumert

SOCIAL RECIPROCITY AND INTERCHANGE IN LONG-TAILED MACAQUES

(MACACA FASCICULARIS)

MICHAEL DAVID GUMERT

Major Professor: Irwin Bernstein

Committee: Dorothy Fragaszy Phillip Holmes Carolyn Ehardt

Electronic Version Approved:

Maureen Grasso Dean of the Graduate School The University of Georgia May 2006 iv

ACKNOWLEDGEMENTS

This research project was supported by a Fulbright Graduate Research Fellowship from

the American-Indonesian Exchange Foundation (AMINEF), Jakarta, Indonesia. I would like to

thank AMINEF for all of their assistance during my stay in Indonesia – especially Nelly Paliama.

I thank the Indonesian Institute of Sciences (LIPI) for providing me with a research permit to conduct research in Indonesia. I am grateful to the Indonesian Department of Forestry for granting me permission to enter Tanjung Puting National Park and to reside in the park area during my research. I would also like to express a deep thanks to Dr. Noviar Andayani from the

Faculty of Mathematics and Natural Sciences at the University of Indonesia for sponsoring my work and assisting in attaining all of my permits.

I give special thanks to my advisor Irwin S. Bernstein for all his assistance in formulating ideas and writing up this research. His critical advice was invaluable to the completion of this work. I would also like to thank my other committee members, Dorothy Fragaszy, Carolyn

Ehardt, and Phillip Holmes for their help and assistance in completing this dissertation.

I give special thanks to my research assistant, Peltanadanson, for his tireless efforts in the field and for being a good friend. I express my gratitude to the management and staff of Rimba

Orangutan Ecolodge for their support and my housing during the research project. I also thank

Pak Yatno and the Baso family for their support, help, and always providing a place to stay in

Kumai during my long stay in Kalimantan. I give special thanks to Bagus Setiawan and Jogi

Ardana, who are always an invaluable help whenever I stay in Indonesia.

In addition to the people that assisted me during my research, I give a very special thanks

to the Rimba macaques. Without them, none of this work would have been possible. Having

been given the chance to take a short glimpse into their interesting lives, I feel mine has been forever changed. I would like to dedicate this work to them.

Last but not least, I would like to especially thank my parents and family for their support during my graduate school career. Without their support and encouragement none of this would have been possible. Thank you so much for your love and support during all of this.

TABLE OF CONTENTS

Page

ACKNOWLEDGEMENTS...... iv

LIST OF FIGURES ...... vii

CHAPTER

1 INTRODUCTION AND LITERATURE REVIEW ...... 1

2 SEQUENTIAL GROOMING RECIPROCITY AND INTERCHANGE IN WILD

LONG-TAILED MACAQUES, (MACACA FASCICULARIS) ...... 7

3 GROOMING AND INFANT HANDLING INTERCHANGE IN LONG-TAILED

MACAQUES (MACACA FASCICULARIS): THE RELATIONSHIP BETWEEN

INFANT SUPPLY AND GROOMING PAYMENT...... 42

4 THE RELATIONSHIP BETWEEN SUPPLY OF FEMALES AND MALE-TO-

FEMALE MATING-RELATED GROOMING BOUT DURATION...... 60

5 GENERAL DISCUSSION AND CONCLUSIONS...... 73

REFERENCES ...... 76

APPENDICES ...... 80

A INTRODUCTION TO BIOLOGICAL MARKETS ...... 81

B SUPPORT FOR BIOLOGICAL MARKETS IN PRIMATES...... 88

C ATTITUDINAL RECIPROCITY: A PROXIMATE EXPLANATION FOR SOCIAL

TRADE...... 95

C EXPERIMENTAL WORK ON RECIPROCITY AND INTERCHANGE...... 102 vii

LIST OF FIGURES

Page

Figure 2.1:...... 34

Figure 2.2:...... 35

Figure 2.3:...... 36

Figure 2.4:...... 37

Figure 2.5:...... 38

Figure 2.6:...... 39

Figure 2.7:...... 40

Figure 2.8:...... 41

Figure 3.1:...... 58

Figure 3.2:...... 59

Figure 4.1:...... 72

CHAPTER 1

INTRODUCTION AND LITERATURE REVIEW

Grooming has many potential functions in primates. It has the utilitarian function of

maintenance and hygiene by removing particles and potential parasites from the pelage of the

receiving animal (Freeland, 1976; Hutchins & Barash, 1976; Barton, 1985; Saunders, 1988;

Tanaka & Takefushi, 1993). Grooming reduces tension (Sparks, 1967; Schino et al., 1988) and

can be used as an act of reconciliation (Aureli & van Schaik, 1991; Aureli, et al., 1992; Aureli &

de Waal, 2000). Based on physiological responses observed in animals engaging in grooming, it

appears to be pleasurable to those engaging in it (Keverne, 1989). Finally, grooming is useful in

the social world of primates, and it is possible that grooming may be used to establish

relationships that can produce beneficial partnerships (Dunbar, 1991). It is even possible that grooming may be directly utilized to facilitate the immediate receipt of other social acts (Barrett

& Henzi, 2001). In this dissertation, I will explore this last function of grooming to determine if grooming can be traded directly for other social acts.

Grooming is common and follows reciprocal patterns of exchange in long-tailed macaques (Macaca fascicularis) (Farslow, 1988; Gumert, 2000; Wheatley, 1999). These basic characteristics of grooming patterns make it possible that long-tailed macaques exchange grooming with other social acts. Grooming may act to facilitate reciprocation of more grooming or it may be interchanged with other acts (Hemelrijk, 1990). Under such conditions, it may be useful to model grooming as “payment for” other acts. Acts that grooming could be traded for 2

include more grooming, tolerance, mating and sexual activity, access to infant handling, and

coalition support.

Biological market theory provides a framework to model social trade as if payment for

obtaining social acts is occurring. A biological market perspective suggests that social trades

occur in social markets that are predictable by basic principles of economics (Noë &

Hammerstein, 1994). A social market is a system of interacting partners that can trade social acts and services. It is predicted that individuals within a social market are seeking partners that can offer social acts and services they demand or need, called social commodities. Individuals must offer some form of payment to the individuals from which social commodities can be obtained.

In this dissertation, I will be investigating whether social acts exchanged in social trades truly can be considered a form of payment or not.

In a social market, a system of social trade will emerge where two different classes of social partners exist (Noë, 2001). One class holds access to a social commodity (i.e. holding class) and the other class seeks access to the commodity (i.e. demanding class). The dynamic

between the two classes will lead to a system of exchange where the demanding class offers

something to the holding class in order to gain access to the desired social commodity. This system of trade would follow the basic principles of economy and factors such as supply, demand, and advertisement will influence the basis of theses exchanges (Noë & Hammerstein,

1995; Noë, 2001). For example, the relative abundance (i.e. supply) of a type of partner should alter what the demanding class will offer to the holding class. When scarce, the demanding class should “pay” more to the holding class, and when abundant should offer less.

Biological markets could account for grooming exchanges and it may be possible to explain some of the reciprocation and interchange observed with grooming by taking this 3 approach. In order to demonstrate that some grooming exchanges can be accounted for by biological market theory, two things need to be demonstrated. First, a clear association between a given act of grooming and a subsequent reciprocated act must be demonstrated. Secondly, it must be demonstrated that principles of economy can influence observed reciprocal exchanges of grooming with other social acts.

Past research on chacma baboons (Papio cynocephalus) has indicated that biological market predications can account for social exchanges (see Appendix B). In one study, it was discovered that when high food competition causes more aggression the demand for tolerance may influence group level patterns of grooming reciprocation and grooming/tolerance interchange (Barrett & Henzi, 2001). It was found that in groups where high food competition occurred, grooming reciprocation occurred less often, indicating a possibility that interchanges of grooming for tolerance were occurring. In groups where low food competition occurred, grooming reciprocation was more common, which is what would be expected if grooming/tolerance interchanges were not occurring. These results led Barrett and Henzi (2001) to conclude that in groups with high levels of food competition, more grooming was directed to interchanges with tolerance than in groups with low food competition. In these groups with lower competition, grooming reciprocation was more common because there was no strong demand for tolerance under those conditions. This study provided evidence that patterns of grooming reciprocation and interchange can be influenced by the current need for tolerance (i.e. demand).

In a second study on chacma baboons, it was discovered that grooming/infant handling exchanges occur and that they seem to be influenced by the supply of available infants in the group (Henzi & Barrett, 2002). Females that groomed mothers with infants did not receive 4 grooming reciprocation, but rather gained access to the mother’s infant. Additionally, the number of infants in the group was negatively related to the average duration of grooming that occurred between females and mothers with infants in relation to infant handling. This supply effect was only observed when females groomed lower-ranked mothers and it was speculated that influences from the dominance hierarchy have the potential to alter basic influences of supply and demand on social exchange.

These past studies suggest that biological market influences may account for some exchanges with grooming. It may prove productive to investigate whether biological market predictions hold up in studies of other species and under differing conditions. It is important to note that these past studies by Henzi and Barrett focused mainly on group level parameters, such as general food competition in a group or the total number of infants in a group. Their studies did not focus on the immediate conditions surrounding specific instances of social exchange. Group level parameters can be used to test biological market theory, but it also should be taken into account that the social exchanges being assessed really occur in the immediate sense. Grooming is given and other acts are immediately returned. If trades with grooming truly occur as such, market influences on those sorts of exchanges should be better observed if looked at in the proximate context of each interaction. In this dissertation, I will be exploring how grooming may be exchanged immediately with other social acts and also how the immediate social context surrounding a grooming interaction can influence the bout’s duration.

Although this study will test whether biological market theory can predict the basic patterns of social exchange, it will not determine if the animals are really capable of understanding value-for-value trade between two social commodities. This is because biological market theory explanations of social exchange should be viewed as the evolutionary result of 5

selection for efficient social exchange and not as accounts of the mental processes of individual

organisms. A biological market explanation should not be confused with an argument that

animals possess a decision making processes that includes an understanding of trade and the

value of social acts.

A better explanation for the proximate influence on social exchange may be attitudinal

reciprocity (de Waal, 2000). Attitudinal reciprocity offers a proximate explanation for social

trade where trade is accounted for by positive social attitudes that could occur after receiving

positive social acts. For example, after a macaque receives grooming, pleasurable physiological effects (see Keverne, 1989 for the physiological effects of grooming) may promote positive attitudes or emotions in the receiver towards their partner that can promote subsequent reciprocation and interchange. This immediate proximate influence may directly cause social trade, while the trade will still follow basic economic models of social exchange. Attitudinal reciprocity may be a proximal mechanism that could produce the economically efficient system of social trade predicted from biological market theory.

In this dissertation, I will try to demonstrate that social exchange follows the predications of biological market theory. I will attempt to demonstrate that grooming can be linked to the immediate reciprocation and interchange of subsequent social acts. Specifically, I predict that

grooming will promote the subsequent reciprocation of more grooming or interchange with

tolerance, sexual activity, and infant handling. I will also attempt to demonstrate that the supply

of available partners capable of offering a particular social commodity can influence the amount

of “payment” in grooming an individual will offer. Specifically, I predict that the supply of

infants will influence female-to-mother grooming durations during interactions involving infant 6 handling and that the supply of females influences male-to-female grooming durations during interactions involving mating.

CHAPTER 2

SEQUENTIAL GROOMING RECIPROCITY AND INTERCHANGE IN WILD LONG-

TAILED MACAQUES, (MACACA FASCICULARIS). 1

______

1Gumert, M.D. Submitted to Behavioral Ecology and Sociobiology, 11/02/05 8

Abstract

Social grooming is a common and potentially valuable act within long-tailed macaques.

Consequently, grooming may be traded reciprocally or interchanged with other acts such as

tolerance or sexual activity. Social exchange related to grooming may be contingent on specific

acts of grooming, and thus traded, or may just be by-products of social relationships. I analyzed

sequences following grooming bouts to test the hypothesis that reciprocation and interchange can

be linked to specific acts of grooming. In contrast to this hypothesis, reciprocation would not

necessarily be linked to specific acts of grooming if social relationships account for reciprocity.

Grooming, aggression, and sexual activity were scored in 10-minute focal and post-grooming

(PG) samples, collected from 38 adults and juveniles. Baseline and PG data were compared

using a variation in rate analysis. Additionally, 73 PG samples from 26 individuals were matched

with control samples. This was to rule out partner preference and motivation to groom, to isolate

the effect of grooming on subsequent exchange. Male-female grooming reciprocation and interchange with sexual activity was tested using a variation in rate analysis on 14 females and 5

males. I found that receiving grooming increased an individual’s grooming toward their partner

relative to baseline and matched-control conditions. Rates of grooming towards third parties decreased following the receipt of grooming. Aggression towards one’s partner decreased after receiving grooming, but not to third parties. Grooming did not increase after male-to-female grooming, but did increase after female-to-male grooming. Instead, after male-to-female grooming, sexual activity increased with one’s partner, but did not with third parties. After

female-to-male grooming, the rate of mating decreased. I concluded that social grooming can 9 facilitate social reciprocation and interchange and thus some social exchange can be shown to be contingent on specific acts of received grooming. 10

Introduction

Long-tailed macaques (Macaca fascicularis) engage in significant amounts of social grooming, and patterns of reciprocation and interchange (see Hemelrijk, 1990 for definitions) are easily detectable with grooming (Aldrich-Blake 1980; Farslow 1987; Gumert, 2000; Wheatley

1999). Based on these two characteristics of long-tailed macaque society, individuals could potentially trade valuable social acts with grooming in sequential exchanges. It is unclear whether primate grooming is valuable in the altruistic sense (Dunbar & Sharman 1984), but grooming does seem to have many immediate benefits to the receiver and therefore could be valuable for immediate trade. Potential values of grooming include maintenance and removal of parasites from the pelage ( Freeland 1976; Hutchins & Barash 1976; Barton 1985; Saunders

1988; Tanaka & Takefushi 1993), pleasure (Keverne et al. 1989), and lowering of social tension

(Sparks 1967; Schino et al. 1988). If grooming does facilitate social trade, it should be possible to detect a temporal relationship between receiving grooming and offering other social acts after analyzing sequences following social grooming.

Several sorts of exchanges could occur following acts of social grooming. First, grooming may be exchanged for more grooming (Henzi & Barrett 1999). Second, grooming may be exchanged for tolerance, which is the absence of aggression towards one’s partner (Henzi &

Barrett 1999). Third, grooming could be exchanged by males for sexual activity with females

(Hemelrijk et al. 1992; Barrett & Henzi 2001). It would seem likely that males would be more apt to exchange grooming with sexual activity than females. First, sexual access may be the most important resource to male primates (Wrangham 1980). Second, male grooming of females is often associated with mating season and estrus (see Goosen 1987). Third, male long-tailed macaques generally are the ones that maintain sexual consortships with females (van Noordwijk 11

1985) and initiate sexual activity. Finally, females are less frequently receptive to sexual activity than males are. Consequently, it would be in the greater interest of males to use strategies such as

grooming to facilitate sexual activity than it would for females.

Several explanations of reciprocation have modeled reciprocity and interchange as pay

backs that are contingent on past specific social action that has value or is altruistic to the

receiver. These explanations include, reciprocal altruism (Trivers 1971), tit-for-tat cooperation

(Axelrod & Hamilton 1981), and biological market theory (Noë & Hammerstein 1994; Noë &

Hammerstein 1995; Barrett et al. 1999; Henzi & Barrett 1999). These all account for trades in

terms of each act’s value. Attitudinal reciprocity (de Waal 2000) also models reciprocity as being

contingent on specific acts, but suggests that a transient positive orientation in the recent receiver

drives that individual to subsequently reciprocate independently of any calculated payback related to the value of specific acts. Alternative to trade of specific acts, reciprocation may not be contingent on specific social acts or facilitation of attitudes. Rather, social relationships may just naturally lead to reciprocal patterns that are the result of bidirectional input occurring over time between partners (Cooper & Bernstein 2000; Matheson & Bernstein 2000).

If social bonding naturally leads to a symmetrical exchange of social behavior without the direct trading of acts, then patterns of reciprocation would be generated independent of any influences of the timing of social grooming. Reciprocity based on social bonds would be the result of familiar individuals repeatedly pairing up during opportune time periods for social

activity (Matheson & Bernstein 2000) and not based on what either individual has received from the other. This would produce reciprocal patterns, but the observed reciprocity would not be

based on direct social trade and thus not be true reciprocity. In contrast, if specific acts of social

grooming can be traded or can influence reciprocation, a temporal association between the giving 12

of grooming and receiving of grooming, tolerance, or sexual activity should be observable. This would indicate that a reciprocated act can be contingent on an initial act of grooming.

In order to link two acts temporally and determine if true reciprocation exists, it is

necessary to demonstrate that one social act is related to increased rates of subsequent

reciprocated social acts. Linking two acts is often difficult and this is especially true as the time

lag between the two acts becomes increasingly large. To better identify true reciprocation, I

observed sequential exchanges following grooming to see if grooming affected the rates of immediate subsequent acts in a fashion predictable by reciprocation and interchange. After one individual gives to another, the receiver can immediately return a social act, end social activity, or interact with a third-party. If reciprocation is occurring, rates of interaction that involve the immediate reciprocation of another social act towards one’s partner should increase and rates of interaction with third parties should decrease. Additionally, receivers of grooming should groom their partner at a higher rate than their partner grooms them, showing a ping pong effect of reciprocation.

In this study, sequences following single acts of grooming were studied in long-tailed macaques. The purpose of the analysis was to determine if receiving social grooming affected an individual’s tendency to reciprocate by increasing rates of behavior towards their partner and decreasing rates towards others. I used a variation in rate method to test for differences in rates of social activity between baseline conditions and time periods following acts of grooming. I additionally used a matched-control method that compared baseline to post-grooming situations, but isolated the effect of receiving grooming on any subsequent reciprocation by controlling for partner preference and motivation to groom.

Methods

Study group and site

Data were collected between June of 2003 and Feb 2005 on the social behavior of a

natural group of long-tailed macaques inhabiting an area in the northwestern portion of Tanjung

Puting National Park (TPNP). TPNP is a 304,000 ha reserve located in the southwestern part of

Kalimantan Tengah (Central Kalimantan), Indonesia at 112o E latitude and 3o S longitude

(Galdikas & Shapiro 1994; PHPA 1994). The study group’s size fluctuated between 48 and 53

individuals, and approximately half of the macaques were immature. There were 19 adult females and 5 adult males. All individuals were recognizable to the researchers through

identifying facial characteristics. The macaques resided in a 1-1.2 km2 home range within the

study site. It was located along the Sekoyner River near the Rimba Lodge, an eco-tourist facility

designed to house visitors to the park. The macaques were inconsistently provisioned by the

lodge from discarded refuse.

Data Collection

The group was followed 5-7 days a week throughout the study with some breaks over a

20-month observation period. With the aid of a trained and reliable (i.e. 90% agreement) field

assistant, I collected ten-minute focal subject samples (Altmann 1974) throughout the day

according to a predetermined randomized list. When a macaque that was listed among the first

five on the randomized list came into sight, a sample was immediately started. During these

samples, grooming, aggression, and sexual activity involving the focal subject were recorded

(see below for definitions). I varied the time of collection periods from day to day to ensure that 14 no time effects confounded the data. I also arranged to have a proportional amount of samples on each individual for each major time period during the day; morning, afternoon, and evening.

I also collected post-grooming samples (PG) with the aid of my assistant. These were special focal samples that were taken on the receiver of an act of grooming for a ten-minute time period immediately following the cessation of a grooming act. A grooming bout was considered over if there was a 30 second time period with no grooming activity, if there was a change in direction (i.e. B starts grooming A), or if the grooming became directed to a third party. During

PG samples, grooming, aggression, and sexual activity that involved the subject were scored.

Time schedules were pre-determined to collect PG samples. During a PG collection period, the first grooming bout that occurred was used to begin a PG sample. When that sample was finished, the researchers waited until the next grooming bout occurred before beginning a new sample.

During all samples, I recorded the occurrence and direction of all instances of grooming, aggression, and sexual activity. I also scored the durations for acts of grooming. Each social act scored is defined as follows.

1. Grooming was an act where one individual manipulated the pelage of another with their

hands or mouth.

2. Aggression was an act that included threatening, charging, chasing, physical hitting, and

biting.

3. Sexual activity included mounting, genital inspecting, presenting of the hindquarters, and

attempting to mount or inspect.

a. Mounting was an act where a male climbed onto the back end of a female,

supported his hands on her back and clasped his feet around the female’s ankles 15

or calves. Once mounting was achieved, the male began pelvic thrusts that would

usually result in intromission and ejaculation.

b. Inspection was an act where a male lifted the tail of a female and touched, sniffed,

or gazed at the anogenital region of the female.

c. Presentation was an act where a female lifted her tail and directed her anogenital

region toward a male.

d. An attempt to mount or inspect was when a male started one of these two

activities but the female moved away before the completion of the act. For

mounting this means the male failed to thrust and for the inspection a male failed

to actually touch or maintain sustained visual contact with the anogenital region.

Analyzing Variation in Rates

I determined each individual’s rate of grooming, aggression, and sexual activity from

focal samples. This rate included interaction by the focal animal with all partners. I also

determined rates of grooming, aggression, and sexual activity for PG samples. I obtained two

rates in PG samples for each activity. First, I determined the rate of activity towards their partner

and second, the rate of activity towards third parties. For grooming, the rate was measured as a

time proportion that indicated how many minutes per hour were spent grooming. For aggression and sexual activity, the rate was measured as the number of acts per hour.

For the first analysis, I used a variation in rate method (de Waal 1987; Judge & de Waal

1997; Sommer et al. 2002). The rates generated from focal samples were used as the expected rates of occurrence of grooming, aggression, and sexual activity and were considered baseline

rates. The rates obtained from PG samples were used as observed rates of activity towards one’s 16

partner and towards third parties. These two observed PG rates, to-partner and to-third party,

were compared with the baseline rates to test for any significant variations in rate. The to-partner

and to-third party PG rates were also compared with each other for significant differences.

Matched Control Tests for Grooming Reciprocation

I used matched control tests (de Waal & van Roosmalen 1979; Aureli 1992) to better

isolate the effect of receiving grooming on directing grooming back to a partner. I used this

second method because it is arguable that the variation-in-rate method may have biased the

grooming-for-grooming exchange analysis. PG grooming samples may represent a biased set of

samples in a social context where grooming is already occurring. This is not the case in the

baseline rate because focal samples were collected in all time periods. Consequently, a bias may

have occurred because PG grooming rates could be higher than baseline rates because the

baseline included samples where the focal individual was not motivated to groom or in proximity

to grooming partners. To rule out these biases, I used a matched control test. In this analysis, I

attempted to match as many pairs as possible of a PG sample and focal sample, or matched

control samples (MC), that had a similar social context.

I ensured that samples represented a similar social context by controlling for motivation

to groom and partner availability. MC samples with the following parameters were used. At any

time during the MC, 1) the two partners from the PG sample needed to come into proximity, and

2) the focal animal needed to express grooming. By doing this, I was better able to isolate the effect of receiving grooming on any subsequent grooming reciprocation because the two major

influences of social bonding on reciprocation were controlled, partner preference (i.e. the partner 17

from the PG sample was within proximity) and motivation for grooming (i.e. the focal individual

expressed grooming).

Statistics

Variation-in-rate analysis

I used paired t-tests to test for significant variation between baseline rates and PG rates of

grooming and aggression for 38 individuals for the following comparisons.

1. baseline grooming and PG grooming to partner

2. baseline grooming and PG grooming to third parties

3. PG grooming to partner and PG grooming from partner.

4. baseline aggression and PG aggression to partner

5. baseline aggression and PG aggression to third parties

6. PG aggression to partner and PG aggression to third parties

I also used paired t-tests to test for significant variation in baseline and PG rates of grooming and sexual activity following male-to-female grooming exchanges for 14 females.

1. baseline grooming rates and PG grooming to partner

2. baseline sexual activity rate and PG sexual activity rate with partner

3. PG sexual activity rate with partner and with third-party males

Finally, for female-to-male grooming exchanges, paired t-tests were used to compare baseline rates of grooming with PG rates of grooming of partners and baseline rates of mounting with PG rates of mounting of partners.

Matched-control analysis

I used a Wilcoxon matched-pair test to test for a significant difference between an

individual’s MC and their PG rate of grooming to partner. Seventy three samples from 26

individuals were analyzed and the number of samples per individuals ranged from 1 to 10. When

there was more than one sample per individual, I averaged the samples for each individual. From

this, I was able to generate an average PG rate and an average MC rate for grooming one’s

partner.

Results

Grooming-grooming exchange

Rates were calculated for grooming interactions from both focal and PG samples to

compare rates. Data from focal samples on all individuals were used to determine the mean

baseline rate of grooming at 4 min 33sec per hour. Data from PG samples were used to

determine the grooming rate towards a focal animal’s partner after the focal animal had received grooming from that partner. These data were also used to determine the rate of grooming to third

parties and the rate of grooming received from the partner (i.e. the initial groomer). The PG rate

of grooming towards partners was 10 min 10 sec per hour which was over two times higher than

the baseline rate of grooming. The PG grooming rate towards third parties was 1 min 56 second

per hour and was less than one half as frequent than the baseline rate of grooming. Finally, focal

animals in PG samples received grooming from the partner (i.e. the initial groomer) at a rate of 5 min 44 sec per hour.

Statistical significant differences were found between these grooming rates for the pre- planned comparisons stated earlier in the methods section. Individuals that had just recently 19 received grooming exhibited significantly higher rates of grooming towards their partner (paired t-test: t37 = -5.231, P < 0.001) and showed significantly decreased rates of grooming toward third-parties (paired t-test: t37 = 5.583, P < 0.001) compared to baseline rates of grooming (see fig. 2.1). The recent receiver also directed significantly higher rates of grooming toward their partner than they received from their partner (paired t-test: t37 = 3.833, P < 0.001) (see fig 2.2).

According to the matched control tests, results were found that were congruent with the above baseline-PG variation in rate analysis results. A PG grooming rate towards ones’ grooming partners (i.e. initial groomer) and a MC grooming rate towards the same partners (i.e. initial groomers in matched PG sample) was determined. The rate of grooming towards one’s partners in MC samples was 8 min 19 sec per hour and the rate in PG samples was 25 min 4 sec per hour. This comparison showed that individuals expressed significantly higher rates of grooming toward their partners in time samples after they had received grooming from their partners, compared to equivalent time periods where the same two individuals came into proximity and the focus individual (i.e. receiver of grooming for PG sample) demonstrated a motivation to groom by exhibiting grooming behavior at some time during the sample (Wilcoxon matched-pairs test: T = 50, N = 26, P < 0.01) (see fig. 2.3). The difference found here represents the isolated effect of the initial act of grooming.

Grooming- tolerance exchange

A baseline rate of 1.03 acts/hr of aggression was calculated from focal samples collected from all individuals. This contrasted with the PG rate of aggression towards one’s partner that they had just received grooming from, which was found to be only 0.027 acts/hr. Additionally, the PG rate of aggression towards third parties was determined to be 0.85 acts/hr. These rates 20

were compared and it was found that individuals expressed significantly lower rates of

aggression towards their partner in samples after they had received grooming compared to

baseline rates of aggression (paired t-test: t37 = 8.014, P < 0.001) (see fig. 2.4). The PG rate of

aggression towards one’s partners was also significantly lower than the PG rate of aggression

towards third parties (paired t-test: t37 = -3.576, P = 0.001) (see fig. 2.4). No significant

difference was found between an individual’s baseline rate of aggression and their PG rate of

aggression toward third parties, indicating that I was only capable of detecting a decrease in rate

of aggression towards one’s grooming partner after receiving grooming but not to other

individuals.

Male-to-female grooming

Variation was found in the sequential exchange pattern of grooming bouts between male- groom-female dyads and female-groom-male dyads. The mean baseline rate of grooming from females to males was calculated to be 7 min 19 sec per hour. The mean PG rate of female grooming towards a recent male grooming partner was 3 min 53 sec per hour. The rates were compared and it could be seen that in samples after male-to-female grooming bouts, females groomed their male partners at a significantly lower rate than baseline (paired t-test: t13 = 3.034,

P = 0.010) (see figure 2.5). Additionally, the baseline rate at which females engaged in sexual activity with males was found to be 1.63 acts/hr, whereas in PG conditions that rate of sexual activity increased to 4.04 acts/hr with the male grooming partners that recently groomed them.

Also in PG samples, females engaged in sexual activity with third parties at a rate of 1.09 acts/hr.

These rates were compared and it was found that females received significantly more sexual activity from their male partner after being groomed than baseline rates would predict (paired t- 21

test: t13 = -2.469, P = 0.028) (see figure 2.6). Furthermore, females received sexual activity at a

greater rate from males that had just groomed them than from third party males (paired t-test: t13

= 4.331, P = 0.001) (see fig. 2.6). These results indicated that male-groom-female interactions did not result in the typical sequential exchange of grooming observed among other dyads, but rather resulted in increased rates of sexual activity.

In time periods following female-groom-male bouts, males groomed their female partners at a rate of 15 min 1sec per hour. Baseline rates indicated that males groomed females at a rate of

1 min 56 sec per hour. The PG rate for male grooming their female partner was a significantly higher rate than baseline, and this was consistent with the general grooming pattern reported in the group level analysis of grooming exchanges (paired t-test: t4 = -5.940, P = 0.007) (see figure

2.7). Additionally, during baseline conditions the rate at which males mounted was 2.12 acts/hr,

but during PG samples their rate of mounting was only 0.64 acts/hr. Mounting was significantly

less frequent after a male was groomed by a female compared to the mean baseline rate of male

mounting obtained from focal samples (paired t-test: t4 = 1.940, P = 0.001) (see fig. 2.8). The

results indicated that female-groom-male bouts promoted grooming reciprocation, but not

mounting, demonstrating an interesting contrast between male-to-female and female-to-male

grooming sequences.

Discussion

This research shows that social grooming in long-tailed macaques can facilitate

immediate reciprocation of more grooming as well as an interchange of tolerance or sexual

activity. Individual macaques groomed their partner more in time periods after receiving grooming from that partner than in baseline conditions or matched control conditions. 22

Furthermore, after receiving grooming, long-tailed macaques groomed their partner more than third party individuals and groomed their partner more than they received from their partner.

Receipt of grooming was also associated with lowered rates of aggression towards one’s partner than baseline, although this rate was not lowered toward third parties. This finding indicates that the receipt of grooming promoted tolerance specific to the individual that just groomed them.

Finally, after receiving grooming from males, females offered lower rates of grooming and received a higher rate of sexual activity from the male that groomed them compared to the female’s baseline rates. Females also engaged in significantly less sexual activity with third parties than they did with their partner. Furthermore, this pattern was not observed after females groomed males. Rather males increased rates of grooming and expressed lowered rates of mounting with their female partner. This contrast clearly shows that male inter-sexual grooming promoted sexual activity and not grooming, while female inter-sexual grooming facilitated grooming and may have inhibited mating.

The data found in this study are in accord with and build upon previous work testing reciprocity. Immediate grooming reciprocation seems to be widespread in many primate species

(see Goosen 1987 for a review; Cercopithecus mitis stuhlmanni: Rowell et al. 1991; Cebus olivaceaus: O'Brien 1993 Papio cynocephalus ursinus: Henzi & Barrett 1999). Grooming has also been found to inhibit aggression and promote tolerance in other species (Old World monkeys: Sparks 1967; Presbytis entellus: McKenna 1978; M. radiata: Silk 1982; Cebus olivaceaus: O’Brien 1993). Interestingly, immediate reciprocation between male-to-female grooming and mating has been less clear, (see Cooper & Bernstein 2000 on M. assamensis for an example), although other past work has provided evidence that grooming is associated with sequences of mating and sexual activity (M. radiata: Kurup 1988). In many anthropoid primates 23

inter-sexual grooming frequencies increase during the mating season and male grooming of

females often increases during female ovulation (see Mitchell & Tokunaga 1976 and Goosen

1987 for a review; baboons: Rowell, 1968; macaques: Jones & Trollope 1968; Drickamer 1976;

chimpanzees Hemelrijk et al., 1992). Other forms of immediate reciprocation that have been

documented include, chimpanzee (Pan troglodytes) food sharing following grooming (de Waal

1997), and M. fascicularis and Cercocebus aethiops appeared to be more inclined to provide

coalition support to monkeys that had recently groomed them (Hemelrijk 1994; Seyfarth &

Cheney 1984).

The conclusion drawn from the results of this study is that reciprocation seems to be

influenced by the receipt of specific acts of social grooming and this influence can be seen

independently of the factors associated with reciprocity due to social relationships. This is not to

say social relationships do not influence social trade; I am only suggesting that we can link a

given and received social act in a manner where the received act seems to influence the observed

reciprocation of the following act. Consequently, social relationships alone are not sufficient to

explain all social reciprocity and a more detailed explanation involving how specific acts

influence chains of social exchange is needed to explain the mechanism of reciprocation (de

Waal & Luttrell 1988).

Possibly a better explanation for the trade of social acts in sequential exchanges is that there could be a system of social commodity trade in long-tailed macaques. In such a system, individuals can be modeled as shopping in a market place for particular partners that can offer social commodities (i.e. grooming, tolerance, sexual activity, etc.) to them (Noë & Hammerstein

1994). To be considered commodities, the acts must have value, be it higher reproductive fitness

(making the exchange reciprocal altruism) or increased success in the immediate social 24

environment. These valued social commodities must be worked for because of their value and an

individual must invest in or pay a partner in order to gain access to a social commodity they are

seeking to obtain. One way of paying could be through social grooming which could facilitate obtaining a social commodity from a partner through true reciprocity – give grooming and then receive another social act. It appears possible that grooming could function as a social tool that

facilitates direct social commodity exchange in long-tailed macaques, and so could potentially be

used in this way.

Although a contingency between reciprocity and social grooming can be detected in this

study, it still remains unclear as to how social grooming facilitates the subsequent trade observed in these sequences of exchange. It would seem quite unlikely that the individuals return acts based on an acknowledgement or understanding of the social value of each act traded. Such a system would require mental bookkeeping and an understanding of debts and payments (de Waal

& Luttrell, 1988, de Waal, 2000). As a result, a biological market explanation may only be useful to explain the evolutionary basis and efficiency of a system of social exchange. It does not explain reciprocation in the proximate sense because it does not illuminate what the true mechanism is in the immediate environment that facilitates reciprocation following an act of grooming.

Attitudinal reciprocity (de Waal 2000) could be the possible mechanism proximately facilitating the observed patterns of sequential trade. Individual macaques do not need to remember exact interactions and trade value-per-value, but rather they form an attitude towards a partner that is based on a specific past interaction, in this case social grooming. Future exchange is contingent on a past exchange but there need not be any understanding of social debts and balances where the animal knows it is returning a valuable act that it owes. Rather, the animal 25

only needs to form positive emotions that are associated with a specific event and partner, which

stimulates the animal to socially interact with their partner (de Waal 2000). Grooming may instill

positive emotions that facilitate social trade through endogenous opiates associated with grooming and social reward (for the physiological affects of grooming, see Keverne et al. 1989).

Research into this area could prove interesting and productive.

The reciprocation observed in long-tailed macaques might work as follows. An act of grooming by partner A to partner B would predispose partner B to behave positively towards A.

The experience of receiving grooming would create a positive orientation of B to A, possibly due to physiological changes caused by the act of grooming itself. B does not need to have a concept that it “owes” a specific amount to A, it only needs the grooming experience to stimulate it into a state where it would likely act positively toward and tolerate A. Succeeding interactions would then be characterized by a tolerance between the two animals. B would be more likely to direct acts to A or allow A to solicit acts (e.g. grooming). Additionally, A could more easily perform acts that B could offer (e.g. sexual activity).

Social relationships, social reciprocity, and social grooming

Kummer (1978) pointed out that social relationships are the major adaptation of primates

that allows them to succeed in the social environment. This argument has been used by others to

capstone positions that social reciprocation is only a by-product of the adaptation of social

bonding and thus is not the result of any special ability to utilize specific acts such as social

grooming to gain advantages in one’s social environment (Cooper & Bernstein 2000; Matheson

& Bernstein 2000). This perspective brings the point of focus to the relationship and not to the

specific acts exchanged. One problem with focusing on social relationships only is that social 26 relationships are the result of how social acts are exchanged. Relationship formation is dependant on the exchange of social acts. Therefore research focusing on specific social acts may be useful to understanding more detailed principles of social exchange.

The term social bond is a category to label individuals that frequently exchange and reciprocate social acts, or in some way exchange acts in a special way relative to others in the group. Therefore, it is the social acts exchanged that are what social bonds are really defined by.

Consequently, explaining and investigating social reciprocity based on the end product only, social bonds, will illuminate little of the finer details of social exchange. Studying how specific observable acts affect social reciprocation will provide us more insight into social exchange than studying how the abstract concept of social bonding influences broader patterns of reciprocation.

My argument here does no give us reason to doubt Kummer’s point that primates have adapted to deal with a social world by evolving the capability of forming and maintaining close social relationships. The question rather is whether the adaptation is the social relationship itself, or is it the traits necessary to develop social relationships. It makes good sense that the need to have social relationships would be the reason why many primate species have been selected to utilize grooming in a social way that provides an individual with the ability to alter their social situation and give the individual the ability to gain from their social partners (e.g. finding grooming partners, avoiding aggression, gaining sexual access, etc.). Social grooming may be a tool for obtaining access to valuable social acts from social partners. Furthermore, there is variation in each individual’s propensity and skill at grooming and potentially “good” groomers may gain more in their social world, over those less adept.

The function of grooming seems to be multifaceted in the world of primates, ranging in utility from simple maintenance to possibly being instrumental in facilitating reciprocation and 27

interchange. Although past research has given us an indication that social reciprocation can be

based on specific received acts of grooming, my research goes beyond the previous work

because it better highlights the immediate contingency between grooming and the subsequent

reciprocation of grooming and interchange of tolerance or sexual activity in one species of primates, M. fascicularis. My work also demonstrates how true reciprocation can occur in the normal social situations of immediate social exchange that long-tailed macaques will encounter each day. This research should focus our attention on observing strings of social action, a method that could prove to be useful for more detailed investigation into the patterns of social exchange.

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Figure Captions

Figure 2.1: In post-grooming samples, individuals groomed their partner significantly more than

baseline levels of grooming would predict and groomed third parties significantly less than predicted by baseline. Black bars represent baseline rates and white bars represent post-grooming rates.

Figure 2.2: In post-grooming samples, recent recipients of grooming groomed their partner significantly more than their partner groomed them. White bars represent post-grooming rates

Figure 2.3: In post-grooming samples, recent recipients of grooming groomed their partner

significantly more than they groomed their partner during matched-control samples of a similar

context where no prior grooming occurred from the partner. The black bar represents the

matched-control rate. The white bar represents the post-grooming rate.

Figure 2.4: In post-grooming samples, recent recipients of grooming expressed a lower rate of aggression toward their partner than their baseline rate of aggression and their PG rate of aggression towards third parties. No significant difference was found between their baseline rate of aggression and PG rate of aggression towards third parties. The black bar represents the baseline rate. The white bars represent the post-grooming rates.

Figure 2.5: In male-groom-female post-grooming samples, recent female recipients of grooming expressed a lower rate of grooming toward their partner than the baseline rate of grooming 33 predicted. The black bar represents the baseline rate. The white bar represents the post-grooming rate.

Figure 2.6: In male-groom-female post-grooming samples, recent female recipients of grooming expressed a higher rate of sexual activity with their partner than the baseline rate of sexual activity predicted. Also, the rate of sexual activity with third party males was significantly less than the rate of sexual activity with their grooming partner. The black bar represents the baseline rate. The white bars represent post-grooming rates.

Figure 2.7: In female-groom-male post-grooming samples, recent male recipients of grooming expressed a higher rate of grooming towards their partner than the baseline rate of grooming predicted. This was consistent with group-level results. The black bar represents the baseline rate. The white bar represents the post-grooming rate.

Figure 2.8: In female-groom-male post-grooming samples, recent male recipients of grooming expressed a lower rate of mounting towards their female partner than the baseline rate of mounting predicted. This contrasts with the increase in sexual activity reported after males groom females. The black bar represents the baseline rate. The white bar represents the post- grooming rate.

Figure 2.1

4 Rate of Grooming (min/hr)

0 baseline to partner third party

Figure 2.2

4 Rate of Grooming (min/hr)

0 to partner from partner

Figure 2.3

10 Rate of Grooming (min/hr)

0 post groom match control

Figure 2.4

1.20

1.00

0.80

0.60

0.40 Aggression (acts/hr) Rate of

0.20

0.00 baseline partner third party

Figure 2.5

Rate of Grooming (min/hr)

0 baseline post groom

Figure 2.6

(acts/hr) of Sexual Activity Rate

0 baseline partner third party

Figure 2.7

6 Rate of Grooming (min/hr)

0 baseline post groom

Figure 2.8

2.5

2.0

1.5

1.0 Rate of Mounting (acts/hr)

0.5

0.0 baseline post groom

CHAPTER 3

GROOMING AND INFANT HANDLING INTERCHANGE IN LONG-TAILED MACAQUES

(MACACA FASCICULARIS): THE RELATIONSHIP BETWEEN INFANT SUPPLY AND

GROOMING PAYMENT.2

______

2Gumert, M.D. Submitted to International Journal of Primatology, 10/26/2005 43

Abstract

Female long-tailed macaques are attracted to infants and often groom mothers bearing

infants. These grooming interactions often involve the grooming female handling the mother’s infants. The grooming may be instrumental in obtaining access to the mother’s infant and it may

be that the interaction is a trade of grooming for infant handling. I attempted to determine if

grooming bouts that involved infant handling can be considered a trade of grooming for access to

the mother’s infant. I analyzed sequences following female-to-mother grooming and interactions

where a female groomed a mother and handled the infant. It was determined that grooming can

facilitate infant handling. It was also determined that the supply of available infants was related

to how long a female groomed a mother. When infants were scarce, grooming interactions were

longer than when infants were abundant. This indicated a possible supply and demand effect on

grooming payment for infant handling. Furthermore, infant related grooming interactions tended

to be unidirectional, where the female groomed the mother, but the mother did not reciprocate grooming. Finally, lower ranked females groomed higher ranked mothers for longer durations

than when higher ranked females groomed lower ranked mothers. This dominance effect

indicated that high ranked infants were potentially worth more. The results are consistent with

the patterns of two commodities being traded as predicted from biological market theory.

Grooming promoted infant handling, while supply and rank position seemed to influence the

degree of grooming payment a female would offer to gain access to an infant. 44

Introduction

In long-tailed macaques (Macaca fascicularis), mothers with infants are very attractive as grooming partners and females tend to group around them and interact with them more frequently than when they are without infants (Wheatley, 1982; Wheatley, 1999). Under these conditions, females may be attempting to groom the mother in an effort to facilitate infant handling. The grooming by the female of the mother could be an interchange of grooming and infant handling. The grooming bout’s relationship to infant handling is indicated by the female’s apparent interest in the infant before, during, or after the grooming bout. These bouts are termed

infant-related (IR) grooming bouts. During IR grooming bouts, females may be thought of as

“paying” the mother in an exchange for access to that infant (Barrett, 2001; Henzi & Barrett,

2002). This biological market perspective predicts that individuals can exchange valuable acts

(e.g. grooming) to gain access to social partners or commodities to which they have limited

access to and/or demand to obtain (e.g. infants) (Noë & Hammerstein, 1994; Noë &

Hammerstein, 1995; Noë, 2001).

Grooming can facilitate immediate reciprocation of other social acts, such as more grooming, tolerance, and sexual activity (see Chapter 2, Gumert, 2005). Given this function of

grooming, it could also immediately promote infant handling. If female grooming of a mother

facilitates access to her infant, then females would be predicted to contact the mother’s infant

more frequently after grooming the mother than compared to times when the mother is with the

infant but has not been recently groomed. The grooming within IR bouts should also typically be

unidirectional and not reciprocal. Thus, the IR interaction should involve the female offering

grooming to the mother and the female gaining access to the infant. The mother is not expected 45 to regularly reciprocate grooming to the female, since the grooming is modeled to be exchanged with infant handling.

Biological market theory goes beyond merely determining if two social acts appear to be exchanged. Market theory predicts that economic forces, such as supply, will influence the dynamics of social exchange by altering the value of commodities. If a grooming/infant handling exchange does exist and market theory can account for the exchange, then the act of grooming associated with infant handling represents a payment that the female gives to the mother to facilitate access to the infant. If the grooming can be considered payment, then it should follow basic economic principles. Consequently, the supply of infants available for infant handling at the time of an IR grooming bout should influence the amount of grooming a female will give to the mother. This prediction is based on a supply and demand model where the rarity of a commodity drives the price (i.e. grooming) of the demanded commodity (i.e. infants) higher.

The payment from a female to a mother was measured by the duration of grooming that she directed towards the mother. This measure was used because the longer a female grooms the more time and energy she would have expended during the interaction. Consequently, it was assumed that the longer a female groomed a mother, the more she was paying during the IR grooming. If grooming can be modeled as a payment and if the supply of available infants truly affects the amount of grooming a female will give to a mother, then the ratio of infants per female should alter the grooming time a female will give to a mother. If a relationship like this was found, it would suggest that the value of infant handling can change in relation to the relative scarcity or abundance of infant partners in the immediate social environment.

The influence of a social economy would certainly not predict all social exchange but merely would be one of many influences on the exchange of social acts. Other factors such as 46 dominance relationships may skew or alter the effects of economic influences, such as supply.

Long-tailed macaques have strict dominance hierarchies that are stable amongst the females

(Aldrich-Blake, 1980; Farslow, 1988; Wheatley, 1999). If a female’s rank can also influence grooming payment during infant-related bouts, then an infant of a higher-ranked mother would be considered to have a higher value on the social market than an infant of a lower-ranked mother. This is because the higher-ranked infant may be more in demand by other females.

Therefore, it is predicted that when females groom up-rank in infant-related grooming bouts, the grooming durations should on average be longer than when females groom down-rank. This would indicate that females will pay more in grooming for access to higher-ranked infants.

A study was conducted analyzing grooming bouts related to infant handling amongst long-tailed macaques at Tanjung Puting National Park. Data were collected on grooming bout duration and the social context surrounding infant-related grooming bouts to test whether there was a relationship between infant supply and grooming duration. Additionally, sequential data following female-to-mother grooming bouts were obtained to determine if grooming facilitated infant handling. Furthermore, the direction of grooming bouts was tested to see if infant-related grooming bouts were typically unidirectional. Finally, the rank direction of grooming was tested to determine if rank influenced grooming duration. I then evaluated the results of these tests to determine if biological market theory could account for the observed patterns of exchange.

Methods

Between June of 2003 and July 2004 data were collected on female grooming interactions that involved infant handling in a group of long-tailed macaques living at Tanjung

Puting National Park (TPNP), Kalimantan Tengah - Indonesia. The study group’s size fluctuated 47

between 48 and 53 individuals, and there were 19 adult females that were investigated during the

study. At any one time, there were between 8 and 13 infants in the group under the age of 6

months, for a total of 24 different infants observed throughout the study. The group’s individuals

were recognized by the researcher through familiarity with each animal’s facial features. The

project was based at an eco-tourist lodge and the group was inconsistently provisioned from

refuse generated by the facilities.

Data Collection

Ad lib sampling was used to collect data on the durations of all grooming bouts between

two females that involved infant handling (Altmann, 1974). These bouts were labeled infant-

related (IR) grooming bouts and were defined as grooming bouts where a female groomed a

mother with an infant. Additionally, immediately before, during, or just after the bout the female

needed to direct attention and physical contact toward the mother’s infant. IR grooming bouts were scored for the total duration of grooming that occurred until the two females stopped interacting and departed from each other. Also, all females and infants within the current social context of the grooming interaction were tallied. Individuals in the social context were all individuals that were within potential sight of the grooming pair.

In addition to ad lib samples, 10-minute focal samples (Altmann, 1974) and post- grooming (PG) samples were also collected. Post-grooming samples were focal samples that were collected on a mother with infant that had just received grooming from a female. During focal and PG samples, touches and contact with the infant being held by the recently groomed mother were scored. To control for biases, focal samples were collected using a randomized method that accounted for the time of day and controlled for potential observer preferences to 48

follow particular individuals. PG samples were also collected on a fixed time schedule and only

grooming bouts that occurred during scheduled PG collection time periods were obtained.

Analyzing the effect of supply on IR grooming bout duration

The ad lib data collected on IR grooming bouts were used to determine if there was a

negative relationship between the current supply of infants in the social context during the

grooming bout and the duration of the female-to-mother IR grooming. To determine the supply

of infants, the ratio of infants per adult female was calculated. This ratio was then matched with the grooming duration of the IR bout and a linear regression analysis was performed. Grooming bouts were scored in minutes and the supply was a value indicating the number of infants/female in the social context of the bout. In this analysis, 113 IR grooming bouts that had complete data on duration and infant per female ratio were put into the regression analysis.

Detecting an increase in infant handling following grooming

Focal and PG data collected from 16 mothers were analyzed to determine if receiving

grooming promoted other females to handle their infants. For this analysis, only focal samples

when the mother was holding the infant were used. Only PG samples where the mother was with

the infant and had just received grooming were used. The rate that the mother’s infant received

contact from other females was then determined from focal samples to generate a baseline rate of

infant contact. The rate of contact from the grooming females to the held infants from PG

samples was then calculated to generate a post-grooming rate of contact with the infant. A

variation in rate analysis was used to determine if the rate of touching towards a mother’s infant 49

was significantly higher in PG samples compared to focal samples. The two rates were then

compared using independent t-tests.

Reciprocal vs. unidirectional IR grooming bouts

IR grooming bouts that contained sufficient data to determine the direction of grooming

were used to determine the proportion of IR bouts that were characterized by reciprocal

grooming and unidirectional grooming. This provided a sample of 138 IR bouts to be analyzed.

From these data, the number and proportion of unidirectional and reciprocal IR grooming bouts

was determined. Following this, a binomial test was used to determine if unidirectional IR

grooming bouts occurred significantly more frequently than chance would predict. The expected

value of reciprocated bouts for the binomial test was P = 0.39, the percentage of reciprocated

grooming bouts that occurred in a random sample of 275 grooming bouts used for post-grooming

analysis.

Determining the effect of rank on IR grooming bouts duration

The ad lib data collected on IR grooming bouts was also used to determine if the rank of

the mother was related to grooming duration. All IR grooming bouts were divided into one of two groups; IR grooming bouts directed up-rank and IR bouts directed down-rank. In up-rank

directed IR grooming bouts the female groomed a higher ranked mother than herself and in

down-rank directed IR grooming bouts the female groomed a lower ranked mother than herself.

An independent t-test was used to determine if the up-rank group’s mean grooming duration was

significantly longer than the down-rank group’s mean.

Results

Data on 16 females were analyzed to determine the mean baseline rates of contact

towards a mother’s infant in post-grooming conditions and baseline conditions. In baseline

conditions when mothers were with their infants, the mean rate of touches towards these infants

was 0.68/hr. The mean rate of touches towards infants with their mother in conditions following

the mother receiving grooming from a female was 5.68/hr. An independent t-test indicated that

this difference in rates was significant (t-test: df = 15, t = 2.938, p = .010). The rate of infants receiving contact from other females was significantly higher after the mothers had received grooming from those females than during baseline periods (see figure 2.1).

IR grooming bouts were scored for being reciprocal or unidirectional. In reciprocal IR

bouts, both the female and mother groomed each other at some point during the interaction. In

unidirectional IR bouts, only the female groomed the mother and the mother did not reciprocate

grooming. Out of 138 IR grooming bouts, 89% or 123 were unidirectional and only 11% or 15

were reciprocal. A binomial test indicated that unidirectional grooming bouts represented a

significantly higher proportion of IR grooming bouts than the baseline proportion of reciprocated

grooming bouts would predict (binomial test: N = 138, P = .39, p < .001)

IR grooming bouts were also scored for total duration of grooming that occurred during

the interaction and for the number of infants per female in sight of the grooming pair. One

hundred and seventeen IR grooming bouts had sufficient data to be analyzed using these two

parameters. A linear regression analysis was run on these 117 IR bouts. The test indicated a

significant negative relationship between female-to-mother IR grooming duration and the supply

of infants (linear regression: r = 0..409; F = 23.05; p < 0.001; r2 = 0.167, df = 115). This 51

relationship demonstrates that when infants were abundant, grooming durations were shorter;

and that when infants were scarce, grooming durations were longer (see figure 2.2).

An analysis was also conducted to determine if grooming up or down rank influenced the

duration of IR grooming bouts. One hundred and thirty eight IR bouts were categorized as up-

rank grooming or as down-rank grooming bouts. In 83 cases, a female was observed grooming

down-rank, and in 55 cases a female was observed grooming up-rank. The mean IR grooming

duration for up-rank grooming was 4 minutes and 55 seconds and the mean duration of down-

rank grooming was 3 minutes and 24 seconds. A Levene’s test for equal variances indicated that

the variances of the two groups were significantly different. Since independent t-tests assume variances are equal, a t-test accounting for the significant difference between each group’s variance needed to be run. After adjusting for the potential bias of differing variances, it was found that the means of the two groups were significantly different (t-test: df = 85.510, t = -

2.204, p = .030). Up-rank IR grooming bouts were significantly longer than down-rank bouts.

Discussion

The results of this study are consistent with the predictions of biological market theory.

Long-tailed macaque females may trade grooming and infant handling with mothers bearing infants. It was found that female-to-mother with infant grooming facilitated contact with an infant. After mothers with infants were groomed by a female, their infants were contacted at a rate nearly 10 times more frequent than baseline conditions when the mothers were with their infants. Additionally, most IR grooming bouts were unidirectional. In the majority of IR grooming interactions, females offered grooming and received access to the mother’s infant. 52

They tended not to receive reciprocated grooming. Grooming was rarely reciprocated in IR grooming bouts because the grooming was traded with infant handling.

The style of trade observed in long-tailed macaques followed the predictions made if a biological market that was influenced by the general economic principle of supply influenced these grooming/infant handling exchanges. The major predication from biological market theory that I tested in this study was that the supply of available partners should influence exchange by altering the value of the desired social commodity (i.e. infants). I looked at how the supply of infants (i.e. ratio of infants per female) in the immediate social context of an IR grooming bout was related to the duration of grooming a female directed towards a mother. A negative relationship was found between female-to-mother IR grooming duration and the ratio of infant per females surrounding the grooming pair. This relationship indicated that the duration of IR grooming bouts was related to the current infant supply in a manner consistent with biological market theory’s prediction that scarcity of available partners should increase their value, while abundance of partners should decrease their value.

This study also took into account that biological markets are not sufficient to predict social exchange through basic economic principles alone. This is because social exchange can also be influenced by other societal factors that could skew the basic economic value of a partner in a social market. One factor that would have the potential to skew the value of a social partner would be their status in the dominance hierarchy of the group. It could be predicted that high- ranked partners would be more valuable than low-ranked partners and as a result grooming investments should vary accordingly. Indeed, IR grooming bouts where lower-ranked females groomed higher-ranked mothers were of longer duration than IR grooming bouts where higher- ranked females groomed lower-ranked mothers. This difference between grooming durations 53

based on rank could be indicative of the value of these individuals as social partners and the willingness of lower-ranked animals to pay more to interact with the infants of higher-ranked partners. It also is indicative of how a system of social exchange can be skewed to benefit higher-ranked animals, by establishing a situation where they receive more for the social commodities they have to offer than lower ranked individuals.

Other past research has also indicated that the supply of infants can influence the duration

of grooming bouts related to infant handling (Henzi & Barrett, 2002). Henzi and Barrett’s

research on chacma baboons (Papio cynocephalus) measured infant supply based on how many

total infants were in a group and they found that grooming durations were related to the number

of infants in the group. They did not measure infant supply specifically for each IR grooming

bout, as I did in this study. As a result, their findings showing the influence of infant supply on

grooming durations were less convincing and only showed grooming duration variation under

conditions of 1, 2, and 3 infants in the group. They also split their supply data into two groups;

mother out-rank female groomer, and female groomer out-rank mother. When the mother out-

ranked the female groomer, the relationship between grooming duration and infant supply was

reversed because when there were 2 other infants present in the group the mean grooming bouts

were longer than when there was only 1 infant in the group. Consequently, the confounding

results of their study made the relationship of infant supply with IR grooming bout duration

unclear.

In my study, the current supply of infants was taken into account for each grooming bout

and thus my work shows the immediate relationship between partner availability and social

decision making in the current proximate environment. Although more stable group dynamics,

such as the number of infants in the group, can certainly influence social exchange, social 54

markets should be expected to be influenced on a moment-to-moment basis. Individuals should obtain and utilize information on the immediate social and economic condition of each interaction and act accordingly. This may explain why the relationship between infant supply and grooming duration was more evident in my research then in Henzi and Barrett’s (2002) assessment of infant-related grooming and infant supply.

In baboons, a test of all infants in the troop may be adequate because baboons live in a more open and visible environment and thus all infants in the troop may be available for every infant handling interaction. In contrast, long-tailed macaque IR grooming bouts only rarely have all infants in sight because they live in forested habitat where visibility can be obstructed and animals can more easily form into isolated sub-groups at any particular time. Therefore, the available infants per female for each grooming interaction can vary greatly, providing the capability to test immediate supply influences on grooming exchanges that occur in relation to infant handling. By showing variation among individual grooming interactions, market forces are shown to be related to immediate decision making for the unique conditions of each interaction.

Henzi and Barrett (2002) also demonstrated that IR grooming bouts were generally unidirectional. This result was replicated in my study and is further supported from work on wedge-capped capuchins (Cebus olivaceus) (O’Brien, 1993). Henzi & Barrett were able to show that rank distance predicted how long grooming durations would last. If a female was grooming a higher-ranked mother, a greater rank distance was related to a greater duration of time the female groomed the mother. These results are comparable to the results found in my study showing that up-rank grooming bouts were significantly longer than down-rank IR grooming bouts.

The conclusion to be taken from these studies is that the basic economic principle of supply predicts and potentially influences social exchange in primates. Furthermore, female-to- 55 mother grooming seems to directly facilitate infant handling. These two results together indicate that a direct trade of grooming with infant handling occurs in long-tailed macaques. Dominance also influences the grooming payment given by a female to the mother and seems to influence the value of an infant on a social market.

I suggest that studying social exchange from a biological market perspective may prove to be a useful tool in understanding basic proximate influence on social exchange. It may help us to uncover some of the problems associated with ascribing value to particular social acts and partners. The supply of available partners seems to be one particular proximate factor that may influence the value of a social commodity or partner.

References

Aldrich-Blake, F. P. G. (1980). Long-tailed macaques. In D. J. Chivers (Ed.), Malayan Forest Primates (pp. 147-165). New York: Plenum Press.

Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227-265. Barrett, L., & Henzi, S. P. (2001). The utility of grooming in baboon troops. In R. Noë, J. A. R. A. M. van Hooff & P. Hammerstein (Eds.), Economics in Nature: Social Dilemmas, Mate Choice and Biological Markets (pp. 119-145). Cambridge: Cambridge University Press.

Farslow, D. L. (1987). The Behavior and Ecology of the Long-Tailed Macaque(Macaca fascicularis) on Angaur, Island, Palau, Micronesia. Unpublished Dissertation, Ohio State University.

Gumert, M. D. (2005). Short-term Grooming Reciprocation and Sexual Interchange in Long tailed Macaques (Macaca fascicularis) in Tanjung Puting National Park, Kalimantan Tengah Indonesia. American Journal of Primatology, 66(S1), 56.

Henzi, S. P., & Barrett, L. (2002). Infants as a commodity on a baboon market. Animal Behaviour, 63(5), 915-921.

Noë, R., & Hammerstein, P. (1994). Biological markets: Supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral Ecology & Sociobiology, 35, 1-11.

Noë, R., & Hammerstein, P. (1995). Biological markets. Trends in Ecology & Evolution, 10(8), 336-339.

Noë, R. (2001). Biological markets: partner choice as the driving force behind the evolution of mutualisms. In R. Noë, J. A. R. A. M. v. Hooff & P. Hammerstein (Eds.), Economics in Nature: Social Dilemmas, Mate Choice and Biological Markets. (pp. 93-118). Cambridge: Cambridge University Press.

O'Brien, T. G. (1993). Allogrooming behaviour among adult female wedge capped capuchin monkeys. Animal Behaviour, 46(3), 499-510.

Wheatley, B. P. (1982). Adult male replacement in Macaca fascicularis of East Kalimantan, Indonesia. International Journal of Primatology, 3(2), 203-219.

Wheatley, B. (1999). The Sacred Monkeys of Bali. Prospect Heights, Illinois: Waveland Press, Inc.

Figure Captions

Figure 3.1: In time periods following the receipt of grooming by a mother with infant, the infant of the mother was touched at a higher rate from the female groomer than the baseline rate of touches towards the infant by all females when with the mother. The white bar represents the post-grooming rate and the black bar represents the baseline rate.

Figure 3.2: A negative relationship was found between the ratio of infants per female and the length of infant-related grooming bouts.

Figure 3.1

6.00

5.00

4.00

3.00

Rate of Touches (act/hr) Touches of Rate 2.00

1.00

0.00 post-groom baseline

Figure 3.2

25.00 Observed Linear

20.00 Average grooming duration 15.00 (min)

10.00

5.00

0.00

0.00 0.50 1.00 1.50 2.00 Infants per Female

CHAPTER 4

THE RELATIONSHIP BETWEEN SUPPLY OF FEMALES AND MALE-TO-FEMALE

MATING-RELATED GROOMING BOUT DURATION

Long-tailed macaques (Macaca fascicularis) exchange social behavior reciprocally and

in some cases these exchanges may be considered a trade of two social acts (Gumert, 2000). One

such act that seems to be linked with social trade is grooming, a common behavior in long-tailed macaques that is often exchanged in association with other social acts (Farslow, 1988; Gumert,

2000; Gumert, 2005; Wheatley, 1999). One potential exchange with grooming is that it may be traded by males for mating and sexual activity with females (Farslow, 1988; Gumert, 2000;

Wheatley, 1999). In this chapter, I will be investigating whether there is any evidence that

grooming is actually traded for mating in long-tailed macaques.

Evidence has been provided that male long-tailed macaques groom the same females that

they mate with and that they exchange a proportional amount of grooming with mating (Gumert,

2000). Additionally, it has been demonstrated that male grooming of females can immediately

facilitate sexual activity because female long-tailed macaques engage in higher rates of sexual

activity with male grooming partners immediately after they have received grooming from their male partner (see Chapter 2; Gumert, 2005). These findings may indicate that grooming and sexual activity can be interchanged, and that trading grooming for mating may be one strategy that males can use to facilitate sexual activity with females. 61

Grooming has been found to be linked to mating and sexually-related behaviors in

several other species of primates as well. For example, in many anthropoid primates, male

grooming of females increases during female ovulation (see Mitchell & Tokunaga, 1976 and

Goosen, 1987 for reviews; baboons: Rowell, 1968; macaques: Jones & Trollope, 1968;

Drickamer, 1976). This is also true in chimpanzees (Pan troglodytes) because estrus females are

groomed more frequently by males than non-estrus females (Hemelrijk et al., 1992). Hemelrijk et

al.’s (1992) study also discovered that female chimpanzees were groomed more often by males

that they had mated with and that males tended to groom estrus females that they mounted

(Hemelrijk et al., 1992). In bonnet macaques (M. radiata) a strong association was found

between grooming and mating, indicating the potential for social trade between the two acts in

this species (Kurup, 1988). The association pattern between grooming and mating is not always

clear, and although past findings indicate an association between grooming and mating in some

species, other work on Assamese macaques, M. assamensis, has not found a clear link between

male grooming of females and mating activity (Cooper & Bernstein, 2000).

It seems that past research indicates a potential for a grooming/mating interchange. If an interchange does exist, then grooming may be considered to be given by a male to a female in order to facilitate or increase the probability of engaging in mating. A direct trade like this would

allow for a test of biological market theory (Noë & Hammerstein, 1994). Males may gain access

to mating opportunities by offering females grooming, and if grooming is offered by males in

exchange for mating, then males may be using grooming as a “payment” to the female. If

payment in grooming is truly occurring, then we should be able to observe several features

predicted from biological market theory that would indicate this. 62

Biological market theory models systems of social exchange as having commodities (i.e. social acts and services) that are exchanged between individuals in a social market, such as grooming and mating. Exchange will be governed by basic principles of economics, such as supply, demand, and advertisement (Noë, 2001). A system of trade arises because individuals within that market vary in their degree of control over access to social commodities. Classes of social partners exist that offer differing social commodities and as a result trading classes form

(Noë, 2001). Males and females provide a good model of how two classes that offer different social acts and services could trade between one another. One class will have or hold access to a desired commodity (i.e. females control access to mating), and another class will seek to gain access to the commodity by interacting with individuals from the class holding the commodity of interest (i.e. males approach and offer grooming).

In this study, I investigated how males interact with females, and looked at how two different classes of social partners, male and female, exchanged grooming and mating. Females represented an opportunity for mating to males and were considered to be able to control male access to mating by allowing or not allowing males to mount them. Males were considered to be seeking access to mating opportunities and to offer grooming as a means to facilitate and obtain access to mating.

It would seem likely that males would be more apt to exchange grooming with mating and sexual activity than females. It has been argued that sexual access may be the limiting resource for male primates (Wrangham, 1980). Additionally, male long-tailed macaques generally maintain sexual consortships with females (van Noordwijk, 1985) and initiate sexual activity (Gumert, unpublished data). Since males initiate sexual activity more often than females, females do not need to put as much into obtaining opportunities to mate because more often than 63

not they will be presented with more mating opportunities than they need. Finally, females are

less frequently receptive to sexual activity than males because of their monthly cycles, putting a

demand on males to develop strategies that increase female receptivity to mating. Based on these

few premises, it would seem to be in the greater interest of males to use strategies such as

grooming to facilitate sexual activity than it would for females. This is why I have modeled the

exchange as males attempting to obtain mating through grooming and females offering the

potential for mating.

Research has already indicated that male grooming of females can facilitate sexual

activity between the male groomer and the female groomee following a bout of grooming (see

Chapter 2; Gumert, 2005). That fact that grooming facilitates sexual activity does not indicate that a true trade involving payment of grooming is occurring. If a grooming/mating exchange can truly be considered a trade between grooming and the receipt of mating, then the economic principle of supply should influence mating-related grooming by affecting the grooming payment given.

In this study, the payment of grooming was measured by the length of time a male groomed a female in any interaction that involved a mating. The length of grooming is an indication of the time and energy a male invests in a female during an interaction, and thus could be an adequate measure of grooming payment. Grooming bouts that occurred in sequence with a mating were labeled mating-related (MR) grooming bouts. MR grooming bouts were interactions between a male and female where the male groomed the female and at some point during the interaction mated with the female.

If interchanges of grooming and mating are influenced by a social market and grooming is considered payment for mating, then the supply of all available adult females within the 64

immediate vicinity of the grooming bout should be related to the total time of grooming the male

invests in the female during the course of the grooming/mating interaction. To test the hypothesis

that MR grooming durations are related to the supply of immediately available females, data

were collected on the duration and social context of all observed MR grooming bouts. Grooming

bout durations were then compared to female supply to assess whether a relationship exists.

Between June 2003 and July 2004, data were collected on a group of long-tailed

macaques inhabiting the northwestern portion of Tanjung Puting National Park, Central

Kalimantan – Indonesia. From the group of macaques, 5 males and 19 females were observed for

this study and data were collected on interactions that involved both mating and grooming. All

individuals studied for this project were identifiable by facial features. The macaques’ home

range was adjacent to a major river demarking the northwest boundary of the national park. An

eco-tourist facility was inside the home range of this group of monkeys and consequently, the

macaques received random provisioning from the lodge that came from refuse generated by the

guests and staff.

Ad libitum sampling (Altmann, 1974) was used to collect data on grooming duration and

social context for all male-female interactions that involved the male grooming the female and

mating between the two occurring. These interactions were labeled mating-related (MR) grooming bouts and were defined as follows - any interaction where a male groomed a female and immediately before, after, or during the grooming bout, the male also mounted the female.

Any time an interaction like this was observed, the total duration of time the male spent grooming the female during the interaction was scored. Additionally, all males and females within potential sight of the grooming pair were scored. A ratio was then calculated that 65

indicated the number of females per male surrounding the MR grooming bout. This ratio was

used as the measure of supply of females per male at the time of the interaction.

To test whether a relationship between MR grooming bout durations and the immediate supply of available females existed, a linear regression analysis was run on 73 such MR

grooming bout interactions. All bouts that were interrupted by an external factor were discarded

from the analysis. Disturbance included other macaques or humans interrupting the interaction.

The analysis revealed a significant negative relationship between MR grooming bout duration

and the ratio of females per male within sight of the grooming pair (linear regression: r = .298, r2

= .089, df = 71, F = 6.923, p = 0.010) (see figure 3.1). The negative relationship indicates that in

times when females were abundant around the grooming pair, MR grooming durations were shorter and when females were scarce around the grooming pair, MR grooming durations tended to be longer. This relationship is what would be expected if the supply of females influenced the amount of grooming “payment” males gave to females based on scarcity increasing the value of females.

Biological market theory predicts that factors such as the supply of available partners will influence how much one individual invests in another (Noë, 2001). In long-tailed macaques, grooming is one behavior that can be easily assessed from this perspective because it is commonly exchanged with other social acts and it can be measured for its duration, which is a rough indication of the time and energy one partner invests in another. The result of this study indicates that indeed there was a negative relationship between the supply of available females and the duration of grooming a male long-tailed macaque gave to a female during MR grooming bouts. This result suggests that the availability of females in the immediate environment is related to the length of time a male grooms a female during interactions that involve mating. It 66

has already been demonstrated that male grooming of females can increase the rate at which

females engage in sexual activity with their male partners (see Chapter 2; Gumert, 2005). The

two of these findings together provide good evidence that interchanges involving male-to-female

grooming and mating follow the expected patterns of two traded acts. In these cases, grooming

seems to be payment for mating.

Biological market theory may be a good model by which to understand the trading of social acts in primates and other social species. Biological market theory models individuals as being in a social market where they are “shopping” for partners that can offer them the social acts and services they need at the cheapest “payment” they can offer (Noë & Hammerstein,

1994; Noë & Hammerstein, 1995). Social primates, such as long-tailed macaques, should be able to obtain and utilize information in the environment that could indicate the potential value of a partner in any given social situation. One of the simplest indications of value would be the supply of available partners able to offer a particular act. In terms of seeking mating, males should take into account how many females are available before a male decides to invest effort

(i.e. grooming) in any one particular female. If there are several females in the area available to a

male, the male should not necessarily invest large amounts of grooming toward a female in

relation to mating because if the interaction fails to culminate in mating there are several other

opportunities. In contrast, if there a few females relative to the number of males, a male should

invest more grooming in a female because her value is higher due to the limited options to the

male if the interaction fails to result in mating.

Although a biological framework may give us a model by which to understand and predict exchanges of social acts, it probably does not account for the motivation and cognition of the organism. I find it doubtful that macaques would be capable of understanding a social trade 67 in terms of a value-for-value trade of two social acts. Rather, I would argue that the observed social exchanges are the results of much simpler processes similar to attitudinal reciprocity (de

Waal, 2000). Here social exchange promotes attitudes and potentially physiological emotional states in the individual which prompt that individual to respond to the receipt of valuable and pleasurable acts (see Keverne, 1988 on the physiological effects of grooming) by returning a beneficial social act. I would additionally speculate that the effect of supply would work in a similar fashion, where individuals would be more attracted to social partners that are scarce.

When a desired class of partner is relatively scarce, it may promote an attitude or emotional state in the animal that makes them more motivated to seek access to that class of partner than if the class of partner was readily available.

No past research on primates has ever found a relationship between the current supply of females and the grooming investment a male will direct towards a female during specific interactions that involve mating. Past research has shown relationships between grooming investment and supply of other types of partners. For example, a relationship was discovered between the supply of infants and grooming-infant handling exchanges in chacma baboon, Papio cynocephalus, (Henzi & Barrett, 2002) and in long-tailed macaques (see Chapter 3). My study indicates that grooming and mating seem to be traded between males and females. Males offer grooming to females and females offer sexual opportunity back. Furthermore, the grooming durations seem to relate to supply of available partners, another indication that the exchange can be considered a trade of two valuable social commodities; grooming being the payment and mating and sexual access being what is purchased.

Although most likely oversimplified from that actual animal’s cognitive state, biological market theory does give us a working framework to predict social exchange independent of an 68

understanding of the animal’s mental process. Given the economic basis of the theory of

evolution itself (i.e. limited supply), it would be predicted that even systems of social exchange would show evidence of organisms acting in economically efficient ways (Noë, Hammerstein, &

Van Hooff, 2001). This work should lead to more research investigating the effects of partner supply on social exchanges to see how wide spread the phenomenon might be. I would speculate that supply effects go much further than just male/female grooming-mating exchange and

female/female grooming-infant handling exchanges. 69

References

Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour, 49, 227-265.

Cooper, M. A. & I. S. Bernstein (2000). Social grooming in Assamese macaques (Macaca assamensis). America Journal of Primatology, 50, 77-85.

Drickamer, L. C. (1976). Quantitative observations of grooming behavior in free ranging Macaca mulatta. Primates, 17, 323-335.

Farslow, D. L. (1987). The Behavior and Ecology of the Long-Tailed Macaque (Macaca fascicularis) on Angaur, Island, Palau, Micronesia. Unpublished Dissertation, Ohio State University.

Goosen, C. (1987). Social grooming in primates. In G. Mitchell & J. Erwin (Eds.), Comparative Primate Biology, vol. 2B: Behavior, cognition, and motivation (Vol. 2, pp. 107-131). New York: Alan R. Liss, Inc.

Gumert, M. D. (2000). Reciprocity in a Wild Group of Long-Tailed Macaques (Macaca fascicularis) At Tanjung Puting National Park, Kalimantan Tengah, Indonesia: An Analysis of Social Currency Exchange. Unpublished MS, Bucknell University, Lewisburg, PA.

Hemelrijk, C. K., G. J. van Laere, et al. (1992). Sexual exchange relationships in captive chimpanzees? Behavioral Ecology and Sociobiology, 30, 269-275.

Kurup, G. U. (1988). The grooming pattern in Bonnet macaque, Macaca radiata (E. Geoffroy). Annals Of the New York Academy of Sciences, 525, 414-416.

Jones, N. G. B. and J. Trollope (1968). Social behavior of stump-tailed macaques in captivity. Primates 9, 365-394.

Keverne, E. B., Martensz, N. D., & Tuite, B. (1989). Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology, 14, 155-161.

Mitchell, G. and D. H. Tokunaga (1976). Sex differences in nonhuman primate grooming. Behavioural Processes, 1, 335-345.

Noë, R. (2001). Biological markets: partner choice as the driving force behind the evolution of mutualisms. In R. Noë, J. A. R. A. M. van Hooff & P. Hammerstein (Eds.), Economics in Nature: Social Dilemmas, Mate Choice and Biological Markets. (pp. 93-118). Cambridge: Cambridge University Press.

Noë, R. and P. Hammerstein (1994). Biological markets: Supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral Ecology Sociobiology, 35, 1-11.

Noë, R. and P. Hammerstein (1995). Biological markets. Trends in Ecology & Evolution, 10, 336-339.

Noë, R., van Hooff, J. A. R. A. M., & Hammerstein, P. (Eds.). (2001). Economics in Nature: Social Dilemmas, Mate Choice and Biological Markets. Cambridge, UK: Cambridge University Press. van Noordwijk, M. A. (1985). Sexual behavior of Sumatran long-tailed macaques (Macaca fascicularis). Zeitschrift fur Tierpsychologie, 70, 277-296.

Rowell, T. E. (1968). Grooming by adult baboons in relation to reproductive cycles, Animal Behaviour, 16, 585-588. de Waal, F. B. M. (2000). Attitudinal reciprocity in food sharing among brown capuchin monkeys, Animal Behaviour, 60, 253-261.

Wheatley, B. (1999). The Sacred Monkeys of Bali. Prospect Heights, Illinois: Waveland Press, Inc.

Wrangham, R. W. (1980). An ecological model of female-bonded primate groups, Behaviour, 75, 262-299.

Figure Captions

Figure 4.1: A negative relationship was found between the total duration of male-to-female grooming in mating-related grooming bouts and the number of females per male in the immediate social context of the interaction.

Figure 4.1

Observed Linear 30.00

Grooming

Bout 20.00 Duration (min)

10.00

0.00

0.00 2.00 4.00 6.00 8.00 10.00 12.00 MR Female per Males

CHAPTER 5

GENERAL DISCUSSION AND CONCLUSIONS

The results obtained in this dissertation support the predictions of biological market

theory. First, grooming seemed to facilitate immediate reciprocity and interchange with

tolerance, sexual activity, and infant handling. Grooming increased the rates of these acts from

recent receivers of grooming to their grooming partner. Additionally, the increased rates seemed

to be specific to the partner and not generalized increases in rates towards third parties. Second,

grooming durations were related to the supply of available partners. Infant-related grooming bout durations were negatively related to the supply of infants, indicating that grooming from females to mothers during interactions involving infant contact were shorter when infants were abundant, compared to interactions where infants were scarce. The same relationship was found for mating- related grooming bouts and the supply of females. Male grooming bouts towards females during interactions involving mating were related to the effects of supply, and thus were shorter when females were abundant and longer when females were scarce.

Because of these results, it was concluded that social exchange can be predicted by biological market theory and that modeling social trade to fit simple economical models can be valuable in predicting the outcome of social exchange. A simple principle such as supply may be useful in determining the current value of a social act or partner at any given moment based on the current social context of relative availability of partners (i.e. number of sought partners per number of individuals seeking that type of partner). Supply would only be one variable of many for ascribing current value to a social partner and in the studies presented here status in the 74

dominance hierarchy also appeared to influence the value of a partner in a social interaction. Up- rank infant related grooming bouts were significantly longer than down-rank infant related grooming bouts. In this study, value was only measured as the amount of grooming time an individual invested in another. Arguably, the time invested by one partner in grooming another could be a useful indicator of the amount of payment given.

Although the basic predictions from biological market theory tested in this study were supported, it does not mean that long-tailed macaques are capable of understanding the principles tested. It is doubtful that long-tailed macaques are capable of understanding that two valuable acts are traded and that the supply can influence the value. Rather the animal would be acting on some more immediate mechanism producing the patterns observed. Attitudinal reciprocity could be a possible explanation for the immediate sequential exchanges of reciprocation and interchange observed. Grooming may promote physiological changes in the receiver of grooming that prompt them to act positively towards and reciprocate with their grooming partner.

Additionally, the influence of supply may act on a similar proximate influence. A simple principle of scarcity producing greater attraction may be occurring. If only a few partners are around, the scarcity of those partners might make the individuals seeking to interact with partners of that class more attractive to them. Like attitudinal reciprocity, this would be based on

a basic physiological and emotional system as well.

Overall, biological market theory may prove to give us better insight into the basic

parameters influencing social exchange. It seems from this study that social acts can be traded in

sequences of exchange and that the principle of supply can influence the amount of “payment”

one invests into the social exchange. Consequently, I suggest that continuing studies aimed at

investigating social sequences and/or economic influences on social trade may prove to be 75 productive in furthering our understanding on the immediate influences on social reciprocity and interchange.

REFERENCES

(From Introduction, Discussion and Conclusions, and Appendices)

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Aureli, F., & de Waal, F. B. M. (Eds.). (2000). Natural Conflict Resolution. Berkeley: University of California Press.

Aureli, F. 1992. Post-conflict behaviour among wild long-tailed macaques (Macaca fascicularis). Behavioral Ecology & Sociobiology, 31, 329-337.

Axelrod, R. & Hamilton, W. D. 1981. The evolution of cooperation. Science, 211, 1390-1396.

Barrett, L., Gaynor, D., & Henzi, S. P. (2002). A dynamic interaction between aggression and grooming reciprocity among female chacma baboons. Animal Behaviour, 63(6), 1047- 1053.

Barrett, L. & Henzi, S. P. 2001. The utility of grooming in baboon troops. In: Economics in Nature: Social Dilemmas, Mate Choice and Biological Markets (Ed. by Noë, R., Hooff, J. A. R. A. M. v. & Hammerstein, P.), pp. 119-145. Cambridge: Cambridge University Press.

Barrett, L., Henzi, S. P., Weingrill, T., Lycett, J. E. & Hill, R. A. 1999. Market forces predict grooming reciprocity in female baboons. Proceedings of the Royal Society of London B, 266, 665-670.

Barrett, L., Henzi, S. P., Weingrill, T., Lycett, J. E., & Hill, R. A. (2000). Female baboons do not raise the stakes but they give as good as they get. Animal Behaviour, 59(4), 763-770.

Barton, R. 1985. Grooming site preferences in primates and their functional implications. International Journal of Primatology., 6, 519-532.

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Dunbar, R. 1991. Functional significance of social grooming in primates. Folia Primatologica, 57, 121-131.

Farslow, D. L. 1987. The Behavior and Ecology of The Long-Tailed Macaque (Macaca fascicularis) on Angaur, Island, Palau, Micronesia. In: Anthropology, pp. 249: Ohio State University. Freeland, W. J. 1976. Pathogens and the evolution of primate sociality. Biotropica, 8, 12-24.

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Hemelrijk, C. K. 1994. Support for being groomed in long-tailed macaques, Macaca fascicularis. Animal Behaviour, 48, 479-481.

Henzi, S. P. & Barrett, L. 1999. The value of grooming to female primates. Primates, 40, 47-59.

Henzi, S. P., & Barrett, L. (2002). Infants as a commodity on a baboon market. Animal Behaviour, 63(5), 915-921.

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Matheson, M. D. & Bernstein, I. S. 2000. Grooming, social bonding, and agonistic aiding in rhesus monkeys. America. Journal of Primatology, 51, 177-186.

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Stopka, P., & Macdonald, D. W. (1999). The market effect in the wood mouse, Apodemus sylvaticus: selling information on reproductive status. Ethology, 105, 962-982.

Tanaka, I. & Takefushi, H. 1993. Elimination of external parasites (lice) is the primary function of grooming in free-ranging Japanese macaques. Anthropological Science, 101, 187-193.

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de Waal, F. B. M. 1997. The chimpanzee's service economy: Food for grooming. Evolution and Human Behavior, 18, 375-386.

de Waal, F. B. M. 2000. Attitudinal reciprocity in food sharing among brown capuchin monkeys. Animal Behaviour, 60, 253-261.

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Wilkinson, G. S. (1984). Reciprocal food sharing in the vampire bat. Nature, 308, 181-184.

Wilkinson, G. S. (1988). Reciprocal altruism in bats and other mammals. Ethology and Sociobiology, 9(2-4), 85-100. 80

APPENDICES 81

APPENDIX A

INTRODUCTION TO BIOLOGICAL MARKETS

“Market selection” and the properties of a social marketplace

In a biological market individuals select who they will interact with socially. This selection process is called market selection (Noë, 2001) and may be an important component to natural selection because it selects for individuals that are more attractive to others in the market.

As a result, traits that increase social attractiveness and social skill are selected for. This would be adaptive from a natural selection stand point because individuals selected from the social market form more mutualisms, trade partnerships, and/or social relationships. By forming a larger network of relationships, individuals gain fitness rewards. Fitness is enhanced because individuals successful in market selection will obtain more relationships and/or develop social relationships of higher quality. Quantity and quality of relationships may be profitable to an individual from a fitness perspective because these factors may yield the following benefits; greater access to food resources, greater access to mating opportunities, greater survival rates, greater social influence, and their offspring may be given more social support and protection.

Market forces place a premium on evolving traits that would give individuals an advantage in obtaining partners from a market of social competitors competing to form social relationships.

A biological system influenced by market selection must consist of individuals that have tradable commodities (i.e. valuable social acts) that can enhance fitness directly, can help secure fitness enhancing social relationships, and/or can promote success in the immediate social 82 environment. Since valuable commodities are traded, biological markets have properties that are similar to market economies of human beings (Homo sapiens sapiens) where services and goods are exchanged amongst various classes of traders. Noë (2001) describes five general properties that biological markets share with human economic systems as follows.

The first property is that some type of valuable commodity must be traded among individuals. The commodities could include social acts such as grooming, mating, coalition support, or infant handling. It could also include more resource-based commodities such as access to food or safe sleeping sites. The value of the commodity could be its utility for building relationships, securing materialistic goods, obtaining social services, promoting survival, enhancing fitness, etc.

Secondly, certain individuals will have differing degrees of control over a commodity’s availability in the marketplace. The control over commodities will generate trading classes, because some individuals will have or offer a social commodity and others may have no direct access to it and thus will have to trade to receive it. Additionally, the degree of control over a commodity will affect its availability to others, which will directly influence the “price” (i.e. how much of another social act is offered) that must be paid to secure the commodity.

The third property is that trading partners must be selected out of a market of individuals competing to gain social partners. Partner choice is affected by the value of the commodities being offered by any one potential trade partner. Within a social market, individuals are seeking to maximize their payoff from mutual trading and therefore their choice of partner should yield the most profitable relationships. They should select to trade with partners that offer commodities they demand, has value to them, offers the best commodities from the available supply, and is affordable in terms of what they can offer to receive it. Profit could be measured in 83 number of commodities received, the value of the received commodities, and/or the securing of trade partnerships (e.g. social relationships, trade alliances, etc.) in relation to the amount of payment or investment the “buyer” must “pay” (i.e. value/price or benefit/cost). Because individuals will be competing for access to partners that will bring them the greatest profit, there should be competition for the most attractive partners on the market. Competition for the best partners will drive the value of attractive partners higher because individuals will begin to pay more for attractive partners in an effort to out compete others trying to access the same partner.

Fourth, and of most importance is that the price of a commodity is determined by supply and demand. A commodity’s price will be directly related to the relative abundance of the commodity in the market and the number of others trying to obtain that commodity. Supply and demand is what makes the biological market approach to cooperation and mutualism unique amongst other approaches (Noë & Hammerstein, 1994). By applying the concepts of supply and demand to biological market, it may be possible to assign values to biological phenomenon, such as social acts, that have been difficult to assign a value.

Fifth, partners can advertise themselves on the market in an effort to increase their attractiveness to others. The information given from advertiser can be true or false, but what is important is how it influences their attractiveness to others. The ambiguity of advertisement forces individuals to assess the quality and integrity of an advertising signal before making any partner selection and thus individual should also be adapted to be good assessors of partner quality. Advertisement can also affect the price of a commodity because it could lead to a greater demand and higher payment towards the advertising class, if the advertisement is effective.

A simple game of partner choice

In order to introduce the reader to biological market concepts, a simple game constructed by Ronald Noë and Peter Hammerstein (1994) will be presented to illustrate how a biological market may work and how the concept of a biological market may be used to predict the exchange of behavior. The game is a partner-acceptance game and the players are a hypothetical

“boa constrictor” and a “shadow bird.” These two organisms live in a desert environment. The constrictor builds a nest mound out in the open desert to lay its eggs and thus the nest is vulnerable to sun exposure. Shadow birds like to lay their eggs in boa nests and then stand over the nest providing shade to both clutches of eggs. As a result, the constrictor has become dependant on shadow birds to provide shade over their nests with their large fan-like tail.

Additionally, the shadow bird is dependant on the boa because the boa protects all of the eggs in the nest from predators.

This dependency between the two organisms creates a situation where shadow birds must use constrictor nests because the bird’s eggs cannot survive without the boa’s protection. The boa also depends on the bird because the boa’s fitness has a strong, positive correlation with the amount of shade over the nest. The result is a mutualism where both the shadow bird and the constrictor benefit reproductively from forming a symbiotic trade relationship to care for their eggs. Biological markets can be used to assess how partner selection will occur between constrictors and shadow birds in the following game.

Noë and Hammerstein (1994) present a partner-choice game where there are two types of shadow birds for boas to choose – birds with short tails and birds with long tails. Long tails are more costly for a shadow bird to maintain than short tails, but the boa benefits more from a bird with a long tail. Shadow birds on the other hand benefit more from having short tails because 85 they are less energetically costly. This creates a conflict of interest where boas benefit more from pairing up with birds with long-tails, but birds pay less by growing short tails. Shadow birds are thus posed with the “choice” of growing long tails or growing short tails. If they choose to grow long tails they will increase their probability of being selected for by boas, but will incur an energy cost for producing the tail. Alternatively they can opt to produce a short tail to save energy costs, but then they will sacrifice their desirability to boas as a partner.

To begin, a two-player game is analyzed where there is only one boa and one shadow bird and no other individuals in the game. The shadow bird will decide on what tail to offer and then the boa will have to choose whether or not it should cooperate with the bird. To assess the boa and the bird’s choices, the cost and benefits to each are estimated. Under conditions of no shade, the boa’s nest will hatch two eggs on average for each clutch. If there is cooperation, the reproductive success of the boa always increases, but the magnitude of increase depends on the size of the tail that its partner offers. With the shade of a long-tailed bird, six eggs will hatch.

With the shade of a short-tailed bird, four eggs will hatch. Consequently, the reproductive advantages to the boa are rlong = 4 and rshort = 2 and so the boa should prefer a long-tailed partner.

Without a reproductive cost from the tail, a bird can lay six eggs (β). A bird must have a tail though and the bird’s tail confers a reproductive cost to the bird’s potential of six eggs. A short tail is cshort = 1 while the cost of a long tail is clong = 3. Therefore, a shadow bird that pairs up with the boa and has a short tail will hatch five eggs of it own (β - cshort = 5), and a shadow bird that pairs up with a boa and has a long tail, will hatch only three eggs of its own (β – clong =

3). The disadvantage to the boa is that the boa is forced to accept whatever the shadow bird offers because it always does better with the help of a shadow bird. As a result, the shadow bird controls the distribution of the tail commodity and will always select to offer a short tail because 86

this is the bird’s most profitable choice in term of benefit/cost. Since the boa will always have to

choose to cooperate with the shadow bird, the bird should always select to offer the commodity

that will incur the lowest cost for it.

If we modify the game slightly it will fit a market model and here we can see how partner

choice will alter the best choice for the shadow bird. Three players are needed, one boa and two

shadow birds. The two shadow birds represent the smallest market from which the boa has the

opportunity to select a trading partner. The cost and benefit assessment remains the same as in

the two-player game. The only difference is the boa can exert a choice for which partner to

select. Because the boa can choose, the birds are now at a disadvantage. This is because the bird

that is not chosen has nowhere to lay its eggs and will therefore have a β = 0. As a result of this

severe reproductive consequence for a bird not selected by the boa, the birds are under rigorous

competition to be selected for by the boa. Since market forces are at work, the bird will choose

the tail that increases their chance of being chosen by the boa rather than choosing a tail based on

energetic efficiency.

The birds still have a choice on which tail type to offer the boa in the second game. This

choice is made independent of each other and occurs prior to the boa’s selection. The bird’s

choice occurs after the molting season when the birds must re-grow their tail feathers and can

“choose” how much energy to invest in their tail production. After molting and growing their tail

feathers in, the birds will go off and attempt to lay their eggs in the boa’s nest. If both birds offer the same commodity (i.e. both offer short tails or both offer long tails), then there is a 50/50 chance that the boa will select either one of the birds to lay eggs in its nest. If both birds bid differently for the boa’s choice (i.e. one offer a short tail and the second bird offers a long tail),

the boa will always select the long-tailed bird because a long-tailed partner provides the greatest 87

profit to the snake in terms of reproductive success. Because the boa can now choose what

commodity to select, the boa exerts control over the market by creating a demand for a specific

commodity, long tails. As a result of the market’s demand by the boas, the bird’s will always opt

to offer a long-tail because it is the only way they will be guaranteed to have a chance to be

selected by the boa. Selecting to offer only a short tail would be too risky because if the other

bird chooses to offer a long tail the short-tailed bird has no chance of being selected as a trade partner. Consequently, when partner choice is put into the game, the partner choice element of

market selection rather than the cost/benefit element of natural selection could be the

predominant factor influencing the adapted trait of an organism. 88

APPENDIX B

SUPPORT FOR BIOLOGICAL MARKETS IN PRIMATES

The market for grooming reciprocation

Some researchers have tried to explain primate social exchange using biological market models and these models have proven to be useful in accounting for observed behavior. For example, in South Africa, hypotheses generated from biological market theory have been tested

with female chacma baboons (Papio cynocephalus ursinus) (Barrett et al., 1999; Barrett et al.,

2000; Barrett & Henzi, 2001; Barrett et al., 2002; Henzi & Barrett, 1999; Henzi & Barrett, 2002).

In these studies, grooming was modeled as a tradable commodity that was valuable to

relationship formation and for cleaning and maintenance purposes. It was predicted that

grooming would be traded for more grooming and would therefore be reciprocated between

partners.

Grooming reciprocation was tested by investigating whether the grooming time between

partners was time-matched, meaning that both partners contributed equal amounts of grooming

time to the other partner during bouts of grooming. To assess time matching, only immediately

reciprocated bouts of grooming were analyzed. Only immediate reciprocation was considered

because grooming reciprocation with time lags is difficult to label as true reciprocation since

later grooming may have been the result of other factors and not reciprocation. After the time

matching analysis was carried out, it was discovered that grooming pairs do significantly time-

match grooming and thus it was concluded that grooming between partners was reciprocated. 89

Interchanging grooming for tolerance: a changing market

Biological market theory predicts that factors such as the basic need for or availability of

a particular act (i.e. supply and demand) can influence social trade. Based on this premise, Barret

et al. (2002) postulated that the availability of other commodities on the market, such as

tolerance, would affect grooming patterns. It was hypothesized that in situations where dominant individuals could offer tolerance to subordinates, grooming patterns should alter because low- ranking individuals would begin exchanging grooming for tolerance with higher ranked partners

(Barrett et al., 2002; Henzi & Barrett, 1999).

Tolerance could be offered in situations where there is increased contest competition and thus dominant animals direct higher levels of aggression toward low-ranking animals in relation to food competition. The increase in aggression toward low-ranking animals represents a power differential between high and low-ranking animals. As competition increases, it is predicted that the overall power differential will become steeper. This means that as power differentials increase, high-ranked animals will direct more and more aggression towards low-ranked animals.

Whether or not power differentials truly increase as predicted is not as important as measuring the increased rates of aggression. Tolerance is the relaxation of aggression, and thus only a measure of frequency and severity of aggression is needed to assess the demand for tolerance. Under conditions of increased aggression, grooming reciprocation is predicted to be lower because lower-ranked individuals will begin to trade grooming for tolerance and high- ranked animals will not need to reciprocate grooming to individuals of lower rank. Overall, lower-ranked individuals need to invest more energy into relationships with high-ranking individuals in order to avoid receiving aggression due to the heightened food competition. 90

These predictions were tested with chacma baboons at two research sites in South Africa,

the Drakensberg Mountains and De Hoop Nature Reserve. At the De Hoop Nature Reserve, food competition for baboons was greater than in the Drakensberg Mountains. As would be predicted from food competition, rates of aggression were higher among the reserve baboons than in the

mountain baboons (Barrett et al., 1999). The high rates of aggression observed in De Hoop indicated that tolerance may be more valuable to low-ranked animals if higher-ranked animals were directing aggression down the hierarchy. Aggression patterns were assessed and indeed a steep dominance gradient was found in De Hoop, meaning that aggression was mainly being directed down the hierarchy. In contrast, the Drakensberg Mountains baboons demonstrated a shallow dominance gradient, meaning that aggression was not mainly directed down the hierarchy but more evenly distributed up and down the hierarchy.

In De Hoop, tolerance would be a valued commodity to alleviate the pressure of the steeper dominance hierarchy. In Drakensberg, tolerance would not be as demanded because aggression is less of a factor. As a result, there is an opportunity to trade tolerance for grooming in the De Hoop baboons. Rather than observing grooming for grooming reciprocation, the researchers predicted that in De Hoop lower degrees of grooming reciprocity should be observed because more grooming will be traded with tolerance. Grooming reciprocation should be higher in Drakensberg than in De Hoop.

As predicted, there was a greater degree of time-matched grooming among grooming dyads in Drakensberg than there was in De Hoop, demonstrating that there was in fact a lesser degree of grooming reciprocation when tolerance was a valued commodity on the market. In addition to this main finding, data collected on one out of the two De Hoop groups yielded a significant positive relationship between rank distance and the receipt of grooming. This positive 91

relationship between a high rank-distance and the receipt of grooming indicates that higher-

ranked individuals may have received more grooming from their low-ranked partners than vice-

versa. This pattern of grooming between high and low-ranking animals is what would be

expected if low-ranking animals are grooming high-ranking animals “to get” tolerance, because

as power differential increases so does the threat of aggression from the dominant to subordinate

animal.

The relationship between rank-related aggression, tolerance, and grooming reciprocity

was further exemplified in a naturally occurring experiment at the De Hoop Nature Reserve

(Barrett et al., 2002). A flood occurred in May of 1998 and heavy rains suddenly flooded the

lakebed that the baboons of De Hoop Nature Reserve frequently utilized. The change in

environment forced the baboons to move upland into a Mediterranean scrub area. At their new

home, the monkeys adjusted to making use of fynbos vegetation and their feeding strategies were altered.

The shift in home range led the baboons to an area of more distributed food resources and

thus they changed from contest competition to scramble competition strategies. This change resulted in a relaxation of aggression down the hierarchy. Before the flood, the De Hoop baboons

had been observed to frequently utilize the dried lakebed. They fed by digging up subterranean

tubers growing in the bed. This feeding strategy created a high degree of within-group

competition because there was contest over access to digging sites. In their new feeding

condition in the more vegetated area, the monkeys could more peacefully feed on dispersed

vegetation with less direct conflict over small feeding sites.

If the predictions from biological market theory are an accurate predictor of grooming

reciprocity, then the ecological shift observed at De Hoop should have caused the following 92 alteration in grooming exchange patterns. Since aggression was no longer directed mainly down the hierarchy, the demand for tolerance from high-ranking partners was reduced. Consequently, there should be an increase in grooming reciprocity because low-ranked animals will groom less for tolerance under these new conditions. Indeed the ecological shift at De Hoop coincided with this predicted alteration in grooming and dyads did in fact time-match more closely than under the condition of contest competition over tuber sites. Furthermore, when the degree of grooming reciprocation in dyads was related to rank distance no effect on grooming reciprocation was found. This indicated that during the post-flood period, low-rank individuals were not giving more grooming to high-ranked partners like they were in the pre-flood condition of high competition. Before the flood occurred dyads consisting of partners with extreme rank distances tended to have unidirectional grooming in an up-rank direction indicating low-ranked animals were grooming for tolerance.

These results demonstrate that grooming reciprocation was altered in situations where tolerance may be a valued commodity to exchange for grooming. Furthermore, it was demonstrated that when tolerance was potentially more valued during the pre-flood period, low- ranking animals directed more grooming towards high-ranking animals than vice versa. This unidirectional exchange pattern is what would be expected if high-ranking animals were interchanging tolerance for grooming from low-ranking animals.

Grooming for infant handling: The effects of supply

Basic market effects such as supply and demand can influence the trading of grooming as a commodity in a baboon social market (Henzi & Barrett, 2002). Infant handling provides a case in point of how supply can drive the “price” of a commodity, as expressed in terms of grooming 93

“payment” within a biological market setting. A study was carried out at the De Hoop Nature

Reserve to investigate how the availability of infants for infant handling might affect patterns of

grooming reciprocation within a baboon troop (Henzi & Barrett, 2002). Mothers with infants under the age of 3 months were observed and scored for their grooming interactions with non- mothers. It was predicted that non-mothers would interchange grooming with mothers for access to their infants. Furthermore, it was predicted that the supply of infants would determine the length of grooming time necessary to “buy” access to a mother’s infant.

The following results were found. First, non-mothers groomed mothers with infants without receiving any immediate grooming reciprocation from the mother. This suggests that non-mother females were interchanging grooming for the mother’s tolerance of handling her infant. Similar findings where females with infants were observed not to reciprocate grooming

have been found in wild wedge-capped capuchins (Cebus olivaceus) (O’Brien, 1993), further

supporting the possibility that non-mother females might interchange grooming for infant

handling. At De Hoop, grooming bouts that involved infants (i.e. mother was holding an infant) were found to be shorter than non-infant related grooming bouts (i.e. neither partner is holding an infant). The shorter duration of infant-related grooming bouts was interpreted as meaning that non-mothers groomed the mother just long enough to gain access to her infant. The motivation behind grooming was speculated to be a means of obtaining access to the infant and was not meant to engage the partner in a long bout of grooming. The third, and most important finding, was that the supply of infants affected the grooming time necessary to obtain and handle an infant. The greater the supply of infants present in the group, the shorter grooming times were before a female accessed a mother’s infant. When there were only a small number of infants 94 available, non-mothers invested a larger amount of grooming into the grooming bout before obtaining access to the infant. 95

APPENDIX C

ATTITUDINAL RECIPROCITY: A PROXIMATE EXPLANATION FOR SOCIAL

TRADE

Short-term exchange strategies

What drives individuals to reciprocate social acts? Even though a multitude of

approaches have been used to explain social exchanges in animal societies, the mechanism

behind reciprocity remains unclear. Connor (1995) and Henzi & Barrett (1999) have pointed out

that if grooming truly was a traded commodity, demanding and receiving immediate

reciprocation would be the best strategy to avoid cheating. Conner (1995) further points out that

by parceling out your goods, rather than giving everything at once, an individual would be more adept at keeping a partner interested in trading. In congruence with these assumptions, one

should expect to see animals trading commodities immediately and sequentially, rather than

expecting to see long-term payback plans, such as what is predicted by Robert Trivers’ (1971)

reciprocal altruism theory. Parceling and immediate reciprocation would involve short-term

optimization of trade rather than a long-term investment in an unpredictable individual.

Primates seem to deal with social events on a short-term time scale and appear to

optimize their access to partners that hold needed social benefits on a daily basis or even shorter

time frame (Barrett et al., 1999; Barrett et al., 2000; Barrett et al., 2002; Henzi & Barrett, 1999).

Henzi & Barrett’s (1999) work has shown that female P. cynocephalus ursinus most often

immediately reciprocate grooming and so are returning social acts on a very short time scale. 96

Even more specifically, Joan Silk (1982) has shown that individual bonnet macaques (Macaca

radiata) that groom high-ranking individuals are less likely to be attacked during the grooming

bout. These low-ranking animals may be “buying” short-term security when grooming these

powerful individuals and thus are receiving an immediate return benefit from the interaction.

These points show that by following immediate trade strategies animals can take advantage of the immediate situation in short-terms trades. By doing so, individuals are at a lower risk of loss

than if they were to trade with partners for some long-term benefit to be obtained later in time.

In many other situations, non-human primates seem inclined to reciprocate social acts not

long after they have received an original act. Up to ½ of all grooming bouts were reciprocated in

blue monkeys (Cercopithecus mitis stuhlmanni) (Rowell, 1991). P. troglodytes were more likely

to share food with individuals that groomed them up to 2 hours prior to the food-sharing bout (de

Waal, 1997). M. fascicularis have been found to be more likely to provide coalition support to

monkeys that had groomed them within the past 10 minutes (Hemelrijk, 1994). Finally, in a

classic study by Seyfarth & Cheney (1984), a playback experiment revealed that unrelated vervet

monkeys (Cercocebus aethiops) were more likely to respond to the solicitations of aid from

individuals that had groomed them within 30-90 minutes before the solicitation. All these cases

show clear examples of how non-human primates do reciprocate and interchange social acts on a

short-term basis.

These cases lead us to ask whether or not these animals are playing a short-term tit-for-tat

trade strategy. Individual B will cooperate with individual A after A has already initiated

cooperation by offering some initial act. Reciprocation of this sort is favorable to a system of

reciprocity, because it is much less risky to the initial giver. Cheating or defection would occur

less frequently and thus individuals would be more likely to initiate trade sequences. Such 97

exchange patterns produce immediate reciprocation. Although the first act seems to produce the

subsequent reciprocated act, it is unclear what the actual mechanism behind these sorts of social

trades is.

Two hypotheses for explaining social exchange

The mechanisms behind immediate reciprocal exchanges are not easy to account for.

Some argue that reciprocation of specific social acts does not occur, and rather, social relationships, or social bonds, predict the exchange of social behavior (Matheson & Bernstein,

2000). Others argue that the symmetrical properties of social relationships alone do not account

for reciprocal exchange (de Waal & Luttrell, 1988; de Waal, 2000). If social relationships

account for social reciprocation, then partner preference and opportunity or motivation to

exchange are the only necessary components to reciprocal exchange. If social acts can be directly traded though, then a reciprocated act should be directly contingent on the receipt of an initial social act. The contingency of one act on another will be observable temporally, in that the reciprocated act should more frequently occur in time periods following an initial act being received. If social relationships alone account for exchange, then a temporal contingency between two acts is not necessary and rather exchange should be best predicted by availability of preferred partners and the current social context’s influence on social exchange.

The premises of the first argument, or social bonding hypothesis, create a testable hypothesis that will allow us to test ideas about social reciprocation. This is because the social bonding hypothesis does not predict temporal variation in the exchange of social acts based on the receipt of a social act. The social bonding hypothesis is based on a relationship model that predicts individuals will exchange social acts symmetrically with preferred partners, regardless of any recent social acts that they have received. Such symmetry-based reciprocity results 98 because individuals will continually pair up with their chosen partner at times when social exchange is convenient and promoted by the social context (Bernstein, personal com).

Exchanging partners take the current situation and each other’s identity into account when deciding to socially trade. They do not take into account what they have and have not specifically received from their partner in the recent past, and thus any social trade is not based on recently received acts.

The second argument, or commodity exchange hypothesis, adds a temporal element into its predictions. This hypothesis predicts that social reciprocation is influenced by specific past social interactions. The commodity exchange hypothesis suggests trading of social acts is truly occurring. Therefore, its basic prediction is that an initial act of affiliation should increase the probability of a return act of affiliation in the near future by the original recipient (e.g. A→B increases the probability of B→A in the near future). This hypothesis contrasts with the social bonding hypothesis because social exchanges in the recent past should not directly affect the probability of subsequent social acts to occur if social bonding is the primary influence on social trade (de Waal, 2000). Rather, if the social bond is the mediating factor predicting exchange, the expenditure of social acts should be equally probable at any given time where the two animals are in proximity to each other and the contextual situation promotes social interaction. Since roughly, p(A→B) = .50 and p(B→A) = .50 a symmetrically balanced relationship should result after numerous exchanges.

Capuchin food sharing

The results of an experiment by Frans de Waal (2000) on capuchins (Cebus apella) indicated that these monkeys were capable of using a memory of specific past interactions with a 99

partner to modify their future exchange patterns with that same partner. In his study, capuchin

monkeys were tested in pairs to see if food sharing was reciprocated. Two capuchins were put

into a test cage and they were separated by a mesh partition. One of the capuchins (the possessor)

was given a bowl of food. The monkeys were then observed to see if the possessor would bring the food near the non-possessor and allow food taking; a phenomenon de Waal labeled as

“facilitated taking”. The possessor was never forced to take its food near the non-possessor and it would have been just as easy for the possessor to hoard its food away from the other monkey.

Since the possessor could hoard its food resources and not allow the other monkey access to the food, the experimenter labeled any food exchanges that resulted as a low-level form of food sharing. Simply, the possessor of food had the option to facilitate food taking by the other monkey or not.

After the experiment was conducted, it was found that animals were more likely to receive food from the partner they shared with on a different day. Monkeys more frequently

brought food to monkeys that had already brought food to them in the recent past. These results

seemed to indicate that the monkeys were paying back their food “debts”. de Waal (2000) argued

that the evidence seemed to indicate that partners could be influenced by past acts of exchange

by facilitating subsequent reciprocation. de Waal did not think that these trades represented an

understanding of payback though and he referred to the resulting reciprocity as attitudinal

reciprocity, rather than calculated reciprocity. It seemed that past experiences set the tone for

future food exchanges, but it was unclear that monkeys actually paid back specific acts.

100

Attitudinal reciprocity: a proximate explanation for social trade

Attitudinal reciprocity is reciprocal exchange of social acts that is based on past interaction. It is more complex than the simple symmetry-based reciprocity predicted by the social bonding hypothesis, but attitudinal reciprocity is not psychologically-mediated in a way that would be considered calculated reciprocity. Calculated reciprocity is reciprocal exchange based on each individual remembering exact exchanges and repaying those exchanges in an exact tit-for-tat fashion based on a comparable value of the traded acts. In attitudinal reciprocity, individuals do not need to remember exact interactions or pay back exact values. Rather, individuals develop an “attitude” towards a partner based on past interactions. Like calculated reciprocity, there is a memory component to attitudinal reciprocity, but the memory does not need to be the result of mental bookkeeping on the time and value of exchanges. Rather, it only needs to be a memory of the attitude a past interaction promoted in the receiver of a social act.

The capuchin food sharing experiment showed that attitudinal reciprocity may be the mechanism because the original food sharing act by partner A may have predisposed partner B to behave similarly when the two monkeys were put into the reverse situation. It was not necessary that Monkey B remember that it “owed” monkey A any specific amount of food. Rather, after having had a positive experience with monkey A in the recent past, monkey B was just more likely to go through all of the necessary steps that would lead to facilitated taking by B. The resulting attitude in monkey B would promote trade with monkey A because when B would be in a situation where trade could occur with A, B would now trade what it had to offer. The trade would be based on an emotional attraction built through recent cooperation, rather than a mental debt incurred from the exchange. 101

Attitude based trading exchanges would not be the direct result of a mental decision to

provide or withhold services based on past interactions, but would rather be based on innate emotional predispositions that become activated after an individual has received an act of affiliation. These emotional predispositions would motivate animals to exchange, creating a situation similar to tit-for-tat (Axelrod & Hamilton, 1983) where the first exchange positively orients the receiver to subsequently exchange back. A tit-for-tat exchange pattern emerges because after an individual has been positively interacted with it will be more likely to give positive affiliation back. The attitude promoting social trade between the two partners would continue until some external social aspect disrupted the over all attitude between the trading partners. Disruptions could include more desirable partners becoming available, group instability, resource scarcity leading to steeper dominance gradients, etc. 102

APPENDIX D

EXPERIMENTAL WORK ON RECIPROCITY AND INTERCHANGE

There have been several experimental studies that have indicated that non-human

primates and other animals reciprocate and interchange social acts and services. These findings

show that reciprocation can occur in the short-term, anywhere between a few minutes to a few days after the first exchange. Work has shown that M. fascicularis interchange grooming and coalition support (Hemelrijk, 1994). P. troglodytes have been observed to interchange food sharing and grooming (de Waal, 1997). C. aethiops have been demonstrated to respond to solicitation calls from unrelated conspecifics after having been groomed by that individual,

suggesting that vervet monkeys may interchange grooming and coalition support (Cheney &

Seyfarth, 1984). C. apella has demonstrated an ability to reciprocate acts of food sharing (de

Waal, 2000). Research on other animals has shown evidence for reciprocity as well. Vampire bats (Desmodus rotundus) reciprocate blood sharing (Wilkinson, 1984) and male wood mice

(Apodemus sylvaticus) may interchange grooming for information about the reproductive state of females (Stopka & Macdonald, 1999). These research findings will be reviewed, except for de

Waal’s (2000) work on C. apella, which was discussed in Appendix C.

Grooming for support in long-tailed macaques

In 1994, Charlotte Hemelrijk published a study demonstrating that M. fascicularis interchanged grooming for coalition support during an experiment conducted at the field station in Bockengut at the University of Zürich. Triads of non-kin monkeys were separated from a 103

colony of approximately 40 macaques and were kept in a smaller enclosure away from the rest of

the colony to run the experiment. One of the three monkeys of the triad was then lured into a

passage cage where a mixture of seeds and syrup was dropped onto its back. After the food

morsel was placed, the macaque (A) was reunited with the other two monkeys of its triad. The

food morsel was placed on the back of monkey A with the intention to stimulate one of the other

two monkeys to groom it. A 10-minute observation session began at this time and it was

recorded who groomed whom.

After the 10-minute grooming period had ended, a second 10-minute period began where the researchers provoked aggression within the triad. The lowest ranked animal (C) was fed a treat in order to stimulate one of the higher ranked individuals to attack it. Once an attack was provoked, there was a situation where coalition support could potentially be offered. These situations were then measured to determine whether a monkey would be more likely to give coalition support to a monkey it was groomed by during the 10-minute grooming period.

After 400 trials were performed on 80 triads, it was found that the syrup treatment did stimulate normal grooming patterns because after the food was removed grooming often continued. It was also found that only females could be induced into aggression and so the experiment was confined to only mature female subjects. Additionally, no victim support occurred, so only aggressor support was measured and so all coalitions were directed at macaque

C. Acts of coalition support for A-B were then compared under three conditions. The first condition was that A groomed B during the grooming period. The second condition was that B groomed A in during the grooming period. The third condition was when A and B did not groom during the grooming period. 104

Significant differences were found between the three conditions. It was found that

females supported others more often after being groomed by them than compared to situations

where no prior grooming occurred (Agroom→B led to Bsupport→A). The reverse was not found and

females did not give more support to females that they had just recently groomed (Agroom→B did not lead to Asupport→B). This finding indicates that the direction of the initial grooming interaction did play a role in determining whether an individual would offer coalition support.

This experiment demonstrates clearly that macaques are capable of interchanging two different social acts.

Grooming for food in chimpanzees

Frans de Waal (1997) performed an experiment on a colony of twenty chimpanzees (P. troglodytes) at the Yerkes Regional Primate Center’s field station in Lawrenceville, Georgia. In the experiment, it was determined that grooming exchanges influenced the likelihood of acts of food sharing, supporting the hypothesis that grooming and food sharing may be interchanged.

During the experiment, cut branches and leaves were bundled into two monopolizable packets and thrown into the enclosure of the chimpanzees. These food trials were conducted twice a week during the spring and summer months of 1992-1994, and 200 food trials were observed during this period. Before the food trials were initiated, the chimpanzees were observed for a 90- minute time period and any social interactions that occurred were recorded. After the food was thrown into the enclosure, social interactions were observed for a half hour time period following the introduction of the bundles. During the post-introduction observation periods, it was determined who claimed the bundles and these individuals were labeled possessors. Secondly, 105 approaches by non-possessors to possessors, grooming interactions, and any food transfers observed were recorded.

After the data were collected, all sharing dyads were analyzed to see if grooming interactions (Agroom→B) affected the frequency of food transfer (Bshare→A). Food-getting success

(FGS) was then measured, which was the proportion of approaches of A→B where A appeared interested in B’s food and A actually obtained food from B. Furthermore, a correction was made to account for situations where B had food to share, and A had none. This allowed the research to test specifically only those situations where A could groom B and increase its chances of receiving food.

The results were analyzed to determine if A had a higher FGS from B in situations where

A had previously groomed B. It was also distinguished whether or not A’s FGS would be affected by whether B groomed A before the act of food transfer. The result demonstrated that among most dyads in the group, A received significantly more food transfers in time periods that followed A’s grooming of B compared to time periods after B had groomed A or no grooming occurred at all. Another interesting finding was that the increase in FGS was most pronounced in dyads where baseline grooming rates were low, suggesting that individuals without stable grooming relationships may have been using grooming solely to gain access to B’s food.

Grooming for support in vervet monkeys: response to signals

Seyfarth and Cheney (1984) conducted a classical study that demonstrated Cercocebus aethiops might interchange grooming for coalition support amongst unrelated individuals. The study was done on female and juvenile monkeys in three separate groups located at Amboseli

National Park in Kenya. The experiment used audio playbacks of vervet solicitations for 106

agonistic aid to assess the response level of others to these calls in time periods following

grooming interaction versus time periods where no grooming had occurred. First, pairs of

subjects were selected for experimentation and then recordings were made of each individual’s

agonistic aid calls.

In the experiment, these recordings of A agonistic aid call were played back in the

vicinity of animal B when A was out of B’s range of sight. The call was played back in two

differing conditions in the experiment. The first condition was to playback the aid call within 30-

90 minutes after A had groomed B (Agroom→B) for at least 1 minute. The second condition was

to playback the aid call during a situation where no prior grooming had occurred between the A

and B for more the two hours. After the playback, the response of B was filmed. The film was

later analyzed to determine the probability that B would look towards the speaker during the

playback. The intensity of B’s responsiveness to A’s call for aid was measured by how many looks B gave toward the speaker and was considered an indicator of B’s willingness to lend

support to A.

After the data were analyzed, it was determined that kin did not show any significant

difference between the prior grooming and no prior grooming conditions. Kin responded with

equal intensity to the solicitations of their kin under both conditions. On the other hand, non-kin did show a significant difference between these two conditions. The grooming of A→B prior to

the play back of the recording significantly increased the intensity of response that B

demonstrated upon hearing A’s solicitation. The results indicated that among non-kin past

interactions can influence the probability of later interactions, and thus interchange between grooming and coalition support seemed to occur. 107

The interesting result here is that non-kin and kin behaved differently and kin seemed to

be less influenced by recent interactions than non-kin. This suggests that in situations where

affiliation rates occur frequently, future interactions may not be as highly dependent on specific

interactions in the recent past. This does not necessarily mean that reciprocity does not occur

between kin and close associates, but that lack of reciprocation may not be as detrimental to future trade of social acts as in non-kin. These results are consistent with kin selection and reciprocal altruism theories because kin should benefit by aiding each other due to inclusive fitness benefits and should do so regardless of past reciprocation. Non-kin should only benefit from aiding each other if the interactions are reciprocated to balance out any fitness costs incurred from the danger of engaging in aggression to support the non-kin partner.

Blood sharing among vampires bats: reciprocity goes beyond primates

Reciprocation is not only observed in primates and does occur in other animals. For

example, Gerald S. Wilkinson (1984; 1988) has performed work in northwestern Costa Rica on

vampire bats (Desmodus rotundus) and found that these animals reciprocated bouts of food

sharing. During initial field studies, the researcher observed vampire bats in their tree trunk

roosts and observed bouts of blood regurgitation between pairs of individuals. These bouts

consisted of one bat regurgitating blood into the mouth of another bat. Out of 110 observed bouts

of regurgitation, 21 bouts were assessed for reciprocation. A significant portion of the 110 bouts

were not considered for reciprocation because they were from mother to offspring. The

remaining 21 bouts were assessed to determine the degree to which nepotism or past association

could account for the acts of blood sharing. It was found that both kinship and association

patterns had an effect on food sharing. Additional studies at two field sites indicated that bats 108

were often given blood when they were unable to feed on a particular night and that both

association and kinship accounted for this sharing.

An additional study was carried out in captivity to determine how much past association

truly affected blood sharing. In this study, kin relationships were controlled to see if

reciprocation based on specific acts of blood sharing was actually occurring. Four female bats

from the same roost tree at the main study site at La Pacific were captured and housed in a small

cage with three females, one male, and one infant from a cave roost in Santa Rosa. No pairs

shared a common ancestor for three generations, except for one grandmother/grand-offspring

pair. Each night one bat was removed from the group. The rest were allowed to feed on blood for

two hours. Two to twelve hours later, the food-deprived bat was put back into the cage with the

fed bats. After placing the bat back with the others, all interactions for the next two hours were

observed. It was found that bats donated blood most often to individuals that were the closest to

starving and needed it most.

The degree of starvation was measured by fluctuations that occur in each bat’s body

weight when they were deprived of food. Bats that exhibited the greatest degree of weight loss were considered to be at a greater degree of starvation. Thirteen regurgitations to a starving

individual were observed. Twelve of these were between members of the same roost population.

These thirteen sharing bouts were examined to determine whether sharing was independent of

past feeding trials. The results showed that blood-deprived bats were significantly more likely to

share blood with individuals they had received blood from in an earlier feeding trial. This

suggests that unrelated vampire bats base their food sharing preferences on past interactions and

have the potential to share preferentially with those individuals that have at one time shared with

them. 109

Trading grooming for sex information in mice

Pavel Stopka and David MacDonald (1999) at the University of Oxford carried out the final study that I will review in this appendix. These researchers conducted a captive study on the sequential patterns of grooming in wood mice, Apodemus sylvaticus, in an effort to account for why males groomed females much more frequently than vice versa. In this study, it was expected that grooming would function to increase the chances of a male gaining access to a female’s anogenitial region. By gaining access to this region of the female, the male could determine the phase of estrus that the female was in. To test whether males traded grooming with females for sexual access, a captive study was set up to test whether grooming a female increased the probability that a male would explore and sniff the female’s anogenital region. Mice were captured in the Wytham Woods nearby the university, were placed in plastic containers, and then brought back to the laboratory for experimentation. Four males and four females were placed into an enclosure and were video recorded. The video recording was used to monitor the sequences of male→female grooming exchanges to analyze grooming-sexual access exchanges.

Grooming interactions were often initiated by the male attempting to sniff the female’s anogenital region. The female most often responded by turning to bite or by moving away to avoid the male. To maintain proximity with the female, the male would often begin to groom the female after his initial attempt to access her anogenital region. This grooming began around the shoulders and head regions of the female. The male would then slowly begin to groom across the female’s body toward the anogenital region. Once the male approached too closely, the female again would try to avoid the male or bite him. Overall, it seemed there was a conflict where the male preferred access to the anogenital region and the female preferred terminating any attempts to access that part of her body. Despite this resistance towards grooming her anogenital region, 110 the female would accept grooming of other parts of her body. A male that did not groom a female and only attempted to access her anogenital region failed to maintain the interaction with the female and she escaped.

The result clearly demonstrated that a male’s success at gaining access to a female’s anogenital region was highly associated with his grooming of her. The results indicate that the two social acts were interchanged and that sexual access would only be obtained if the males groomed the females. The results seemed to indicate that females only permitted access to their anogenital region after a certain threshold time was reached of the male grooming the female.

The authors argued that what was happening was that females were “bargaining” with males. A female would only allow access to the region of her body the male was seeking out after she received an act that was beneficial to her. Grooming was considered a commodity that could be used to barter with females for reproductive information or sexual access. This study provided a detailed example of the steps that are carried out when two social acts are traded amongst individuals motivated to obtain different outcomes.