Social relationships among adult female baboons

Anita.Behav.,1976,24, 917-938

SOCIAL RELATIONSHIPS AMONG ADULT FEMALE BABOONS BY ROBERT M. SEYFARTH*

Sub-Department of Animal Behaviour, Madingley, Cambridge Abstract. Adult female baboons were studied over a 15-month perigd which included sexual cycling, pregnancy, and lactation. Females could be ranked in a linear dominance hierarchy which accurately predicted the direction, but not the frequency, of agonistic interactions. Females were most attractive to others during lactation, receiving less aggression, more friendly gestures, more grooming, and grooming by more different individuals than females in other reproductive states. In all three reproduetive states high-ranking females were more attractive than others. When differences in behaviour related to changes in reproductive state were factored out, individual females groomed animals next to themselves in the dominance hierarchy more than others. A model is presented showing how rankrelated access and attractiveness may interact to perpetuate this distribution of grooming over time. Despite the increase during the last decade in both field and laboratory studies of primate social behaviour, few observers have concentrated on the behaviour of adult females (but see Rowell 1969). This is somewhat surprising, since adult females are frequently described as the focus of group organization (e.g. Hall 1965; Bernstein & Sharpe 1966), and are generally regarded as the most stable element of primate reproductive units (e.g. Crook I970a). Females are known to play an important role in the transmission of norms and traditions within primate groups (e.g. Itani & Nishimura 1973), while observers of both newly formed and naturally dividing groups of rhesus monkeys have defined the existence of a stable social group in terms of the behaviour of adult females (Vandenbergh 1967; Missakian 1973). This paper considers social behaviour among eight adult female baboons (Papio cynocephalus ursinus, Thorington & Groves 1970), in an attempt to answer the following questions: (1) Do individuals distribute their behaviour at random throughout the group, or can some dyadic relationships be distinguished from others ? (2) How do changes in an individual's reproductive state affect her interactions with others ? (3) What social factors can be shown to affect the overall pattern of interaction among females?

1957 m at its highest point. There are marked seasonal changes in temperature, with occasional snow during the winter months of June, July and August. Annual precipitation averages approximately 36 ore, and occurs primarily between October and April. The Baboon Troop When research began the troop consisted of two adult males, eight adult females, and fourteen other individuals. During the study there were eight births, one death, and four emigrations. Animals were captured and marked with plastic ear-tags which permitted individual identification from a distance. Capturing and marking were done at night, and did not appear to affect either the baboons' behaviour or their degree of habituation (for further details see Seyfarth 1975). Methods of Observation and Recording Two full-time observers participated in this project. Observation sessions were scheduled so as to provide a cross-section of social behaviour throughout the day (see below), and three complementary methods of data collection were used in an attempt to provide both a large sample of data and a fairly uninterrupted record of social behaviour over a 15-month period. The onset and termination of observation sessions. The onset of each day's observation session was determined by the need to collect monthly data equally from four daily 'quartiles': dawn to 09.00 hours, 09.00 to 12.00 hours, 12 noon to 16:00 hours and 16.00 hours to darkness. The length of each observation session was agreed upon before data collection had begun, with observation sessions usually lasting from 2 to 3 hr. Methods of data collection

Methods The Stndy Area Research was carried out from September 1972 until March 1974. The area where the research was carried out consists of rocky, mountainous terrain, rising to an altitude of *Present address: RockefellerUniversity,Field l~esearch Center, Millbrook, NewYork 12545, U.S.A. 917

918

ANIMAL BEHAVIOUR,

described below are defined as in Altmann (1974). Instantaneous sampling. This method was used over a 15-month period to record the location and behaviour of each individual thirty times each month in each of the four daily quartiles listed above. On-the-minute samples were made every minute throughout each observation session. The observer selected a different individual on each minute, using a number of selection procedures which tended to randomize the choice of a target individual (for details see Seyfarth 1975). No individual was sampled more than once in every 10 min. Animals were recorded as either foraging, feeding, moving, sitting, grooming, playing, or engaged in other social behaviour. In the case of social interaction, all other individuals involved were also noted. In addition, records were made of all the animals either touching, within 1 m (approximately arm's length), or within 3 m of the target individual. As used in this study, instantaneous sampling produced a relatively uninterrupted record of the spatial distribution of individuals, and provided a fairly large sample of data on behaviour of long duration (like grooming), but it failed to record either lengthy sequences of behaviour or interactions which occurred at a low frequency throughout the study. Focal animal sampling. This method was used concurrently with instantaneous sampling to record the behaviour of each individual for a total of 3 hr each month. When possible, observation sessions lasted 15 min, and in all cases data collection was divided equally among the four daily quartiles and distributed fairly evenly throughout each month. As with instantaneous sampling, observers employed a number of selection procedures which tended to randomize the choice of target individuals (for details see Seyfarth 1975). Focal animal sampling provided information on the frequency, quality, and context of social interactions, with two limitations. First, in a number of eases the sample produced on each dyad was too small to allow statistical treatment; and second, there were often long breaks between successive samples on the same individual. Sequence sampling. This method was therefore used throughout each observation session to supplement data gathered by the focal animal method. Excluding grooming, all categories of social behaviour among all adult individuals were recorded. Grooming was excluded because a sufficiently large sample of grooming data

24, 4

was produced through instantaneous and focal animal recording (see above); and sequence sampling concentrated only on adult individuals because they were the focus of this research project. Sequence sampling yielded a large sample of data on social interactions, and provided useful information on particular day-today changes in behaviour. In addition, since observers spent a similar amount of time with the troop each month, data from sequence sampling could be combined with data from focal animal sampling to calculate rates of behaviour in cases where the behaviour in question was observed only rarely (see below). The Female Reproductive Cycle: Defmitions Gillman & Gilbert (1946), Rowell (1967), and Hendrickx & Kraemer (1969) have described four easily observable changes in the female baboon's sex skin: inflating, swollen, deflating and flat, which correspond to the early and late follicular and the early and late luteal phases of the menstrual cycle, respectively (see also Hausfater 1975). In a long-term study the onset of pregnancy and lactation can also be determined. In the following sections the reproductive cycle of each female is divided into three reproductive states: sexual cycling, pregnancy, and lactation. The sexual cycle is further divided into four stages: inflating, swollen, deflating and flat. Results: I. Agonistic Behaviour A. ~Definitions Following Rowell (I966), agonistic interactions were divided into two general categories: approach-retreat interactions, and interactions involving aggressive behaviour. Approachretreat interactions occurred when one animal walked to within 3 m of another, and the other moved more than 3 m away. Such interactions were therefore not a measure of aggressiveness on the part of the approaching animal, but an indication of subordination by the avoiding animal (Rowell 1966). Hall (1962), Rowell (1966, 1972), and Hausfater (1975) document the ways in which female baboons have been observed to behave aggressively toward each other. B. Dominance Table I presents data on the frequency and direction of approach-retreat interactions between females during three successive 5-month periods. The direction of interactions was highly predictable, despite changes in every female's reproductive state (see below). Low-ranking

SEYFARTH: SOCIAL RELATIONSHIPS IN FEMALE BABOONS females a v o i d e d others m o s t often, a n d highr a n k i n g females were m o s t frequently a v o i d e d . T a b l e I I presents d a t a o n the direction a n d frequency o f aggression between females d u r i n g the s a m e three 5 - m o n t h periods. A l t h o u g h m o s t b o u t s o f aggression followed the p a t t e r n ' d o m i n a n t threatens s u b o r d i n a t e ' (see above), a n d l o w - r a n k i n g females generally received the m o s t aggression, h i g h - r a n k i n g females were n o t necessarily the m o s t aggressive. R a n k o r d e r a m o n g females in this s t u d y was therefore similar n o t only to t h a t described in o t h e r studies o f b a b o o n s (Rowell 1966; H a u s f a t e r 1975), b u t also to t h a t seen a m o n g female J a p a n e s e m a c a q u e s (e.g. K a w a i 1958),

919

rhesus m a c a q u e s (Sade 1967), s t u m p - t a i l e d m a c a q u e s (Rhine & K r o n e n w e t t e r 1972), p a t a s m o n k e y s (Hall 1967), a n d g e l a d a b a b o o n s ( B r a m b l e t t 1970). C. The Frequency of Agonistic Behaviour F r e q u e n c y o f agonistic b e h a v i o u r a m o n g females was generally lower t h a n t h a t seen either a m o n g males a n d females o r between males (Table III). T h e r e was n o i n d i c a t i o n t h a t frequency o f agonistic b e h a v i o u r in p a r t i c u l a r pairs o f females was related t o the i n d i v i d u a l ' s relative p o s i t i o n s in t h e h i e r a r c h y (el', Bernstein 1970).

Table L Frequency Distribution of Approach-Retrent Interactions Between Adult Females During Three Successive 5-month Periods. Females are Arranged in the Rank Order which Produces the Fewest 'Reversals': Spearman Correlations (rs) Indicate the Extent to which Total Avoids Given and Received in Each Period were Inversely and Directly Correlated with l~nk. Based on 3 hr of Focal Anita! Sampling on each Individual Each Month, thus 6 hr on Each Dyad Avoiding females I-I. (a) January-May 1973 I-I. Wel. Lys. Shir. LP~ PM M Patch Total times avoiding

Wel. 2 2

1

1

Lys.

Shir.

LP

PM

M

Patch

3 2

5 7 3

6 3 1 1

19 3 1 1

7 4

1 4 5 3 5

1

!

1

5

I 6

16

1 2 I

1

12

24

15

23

10

9

10

3

9 1

2 3 6 3 3

Total times avoided 43 23 12 7 rs = 0-95 8 3 P < 0"01 2 0

rs = -- 0.83, P < 04)1

(b) June-October 1973 H

10

Wel. Lys, Shir. LP PM M Patch Total

3

18

1

I1 4

1

2

12 3

1

1

6 2 1 1 4

0

0

10

5 36 rs ------- 0"57, Ns

(c) November-March 1973-74 tt

25

20

27

17

6 1

15

14

12

12

Wel.

3

3

2

3

Lys. Shir. LP

8

1 1

I

3 2

5

11

PM M

75

6 9 1

12 19 12 rs •ffi 0.90 1

1 1

1 P < 0"01 1

Patch Total

63 23 26 12 rs ~= 0.93 7 4 P < 0.01 5

0 0

5

11

26 19 15 rs = -- 0,74, P < 0,05

20

25

920

ANIMAL BEHAVIOUR,

Frequency of agonistic behaviour and changes in reproductive state. (i) Agonistic behaviour and oestrus, Kummer & Kurt (1965) found that female hamadryas baboons received aggression at a higher rate during oestrus than at other times, and Rowell (1967) found that, when the interactions of swollen females were compared with those o f others, a greater proportion of the swollen females' interactions involved aggression. In contrast, Hausfater (1975) found that females received less aggression from others when fully swollen than at other times, at least partly because the swollen females' sexual consorts herded them away from potentially aggressive interactions. During the present study, no changes in the frequency of female-female agonistic behaviour could be correlated with changes either within the sexual cycle or from sexual cycling to pregnancy. This point is discussed further in two subsequent papers (Seyfarth in preparation, a, b), where I also discuss 'herding' behaviour between males and females. (ii) Agonistic behaviour and lactation. Studies of captive rhesus monkeys (Rowell, Hinde & Spencer-Booth 1964; Spencer-Booth 1968), captive baboons (Rowell 1969; see also Rowell, Din & Omar 1968), and free-ranging vervet monkeys (Struhsaker 1971) have shown that lactating females receive many more friendly approaches than females in other reproductive states, and that during lactation such approaches are most frequent when the infants involved are youngest. Baboon females are most likely to avoid friendly approaches when their infants are youngest (RoweU, Din & Omar 1968), while both rhesus and patas monkey mothers are most likely to restrain or retrieve their infants during the first few weeks after birth (Harlow, Harlow & Hansen 1963; Hinde, Rowell & Spencer-Booth 1964; Kaufmann 1966; Hall & Mayer 1967; but see also Rosenblum & Kaufman 1967). Finally, both Hall & Mayer (1967) and Hausfater (1975) indicate that females receive less aggression from others during lactation thart at other times. The arrival of infants can obviously affect the frequency of agonistic behaviour among females in a number of ways. Below I consider changes in the frequency of 'friendly' approachretreat interactions and interactions involving aggressive behaviour. During lactation, there was no change in the frequency of the standard type of approach-

u.~

24, 4

'i

i ~O SEXUAL F CYCLE

7-10 T~-t4 ~5-~8 ~I~-22 23LACTATION, INFANT .t~3.E(WKS

Fig. 1. The number of friendly approaches per month received by each adult female when sexually cycling, pregnant, and during lactation at various infant, ages. N = 7 females through infant age 22 weeks, N = 5 females thereafter. Based on focal animal plus.sequence sampling.

4O n"

b" IX.

Or" LL

0 6 710 1114 1518 19 INFANT AGE (WKS.)

Fig. 2. The percentage of friendly approaches avoided by lactating females at various infant ages. N = 7 'females.Basedon focalanimalplus sequencesampling, retreat interaction, defined above. In contrast, at the start of lactation there was a sharp in9 in the number of 'friendly' approaches, when an approaching female attempted t o touch, hug or kiss the lactating female Or her infant (Fig. 1). Figure 2 shows that lactating females avoided friendly approaches most often when their infants were 6 weeks old or less. It was not unusual to see mothers avoid the friendly approaches of females who were lowerranking than themselves. However, there was no relation between a mother's rank and the frequency with which she avoided friendly approaches at any given infant age, nor did

SEYFARTI-[: SOCIAL RELATIONSHIPS IN FEMALE BABOONS m o t h e r s a v o i d p a r t i c u l a r individuals m o r e often per a p p r o a c h t h a n others. I n o r d e r to d e t e r m i n e the relation between the arrival o f infants a n d changes i n the frequency o f aggression, it was necessary to dis, tinguish between the b i r t h o f a n i n f a n t to the d o m i n a n t female in each d y a d , a n d the b i r t h o f an infant to the subordinate. D o m i n a n t females were generally m o r e responsible t!lan s u b o r d i n a t e s for the initiation o f aggression in each d y a d (Table H ) . Seventeen d y a d s were o b s e r v e d t o m a k e the transition f r o m ' b o t h individuals p r e g n a n t ' to ' b o t h lactating'. F i g u r e 3 illustrates the m a n n e r in which the arrival o f infants affected the frequency o f aggression in each pair.

921

T w o p o i n t s are relevant to an i n t e r p r e t a t i o n o f Fig. 3. First, a change in the rate o f d y a d i c aggression was defined as a n alteration greater t h a n or equal to 0.04 interactions p e r h o u r (roughly a 30 p e r cent change: see T a b l e III). This is a crude m e a s u r e o f changes in the frequency o f aggression, a n d m a y well u n d e r estimate changes in b e h a v i o u r related to birth. Second, in m o s t pairs o f females t h e arrival o f one infant b r o u g h t a b o u t a decrease in the rate o f aggression, regardless o f w h e t h e r the subo r d i n a t e o r the d o m i n a n t female gave birth. W h e n a p a i r c h a n g e d f r o m having one lactating female t o having two, however, n o further change in aggressive b e h a v i o u r was observed.

Table H. Frequency Distribution of Interactions Involving Active Aggression Between Adult Females During Three Succeessive 5-month Periods. Legend and Data Collection as in Table I

Females receiving aggression H.

Wel.

Lys

Shir.

LP

PM

M

1 1

1 1

6

3 :3

1 2 2

(a) Januar)~-May 1973 FI

Wel. Lys. Shir, LP PM

2 1

1 1

M

2 1

2

(b) June-October 1973 H Wel. Lys. Shir. LP

5

9

t 1 1

6 8 7 rs = -- 0.83, P < 0i01 1 1

3

1

2 2

2 1

1

1

15 9

2 1

3

7

1

2 1

2

5

11

3 6 5 7

3 1 2

Patch 1

4

8 P < 0"01

4 8 14 7 rs = 0'60 10 1 Ns 2 1

i 0

9 t2 rs ~ 0 . 9 0

16

1

PM M

Total

1 1

1 1

Total times aggressive

2 3

1

Patch Total times avoiding aggression

4 5

Patch

5

4

5

22

6

rs ------- 0.92, P < 0"01 Total

(c) November-March 1973-74 H Wel. Lys. Shir. LP PM M : Patch Total

3

6

1

0

2

2 2

1

1

1

2 I 0

0

5

0 2 1 rs = -- 0.68, P < 0.05

4 4 rs = 0.56 2 2 NS 1 0

922

ANIMAL

BEHAVIOUR,

Data thus suggest that infants both inhibited aggression which would otherwise have been directed at their mothers and inhibited their mothers' tendency to behave aggressively toward others. D. T h e Social Context of Agonistic Behaviour Definition. The social context of any interaction may be described in terms of the presence and/or behaviour of other, nearby animals when the interaction occurs. Specifically, in this study an agonistic interaction between females was said to have occurred 'over access to an adult male' if the avoiding/threatened female was alone near a male or grooming or presenting to him, and the approaching/threatening female then stayed near or groomed or presented to the same male. Similar criteria were used for agonistic interactions 'over access to the handling of an infant' and those 'over access to the grooming of a lactating female'. Female aggressive 'strategies'. If female A is 'attempting' to supplant female B when the latter is near or interacting with a desirable object, female A may be thought of as having two alternative 'strategies' open to her, provided that A is dominant over B. Female A could simply approach, relying on B, as the subordinate animal, to move off. This would probably achieve the desired result with a minimum of social disruption. Alternatively, female A could threaten or chase B away. Data in Table IV suggest that females did in fact use different aggressive 'strategies' in

/

Both

Sub. ~.lact. Dom.~4) preg. ----..N = 8 i:lyads 6 decrease 2 increase

Both .~ Q lactating N =8 dyads 8 no change

24,

4

different social contexts. In competition over adult males approaching and threatening were equally likely, while in competition for access to infants and lactating females approachretreat interactions were relatively more frequent. T o examine further the conclusions suggested by data in Table IV, behaviour in the twentyeight possible dyads was compared in different social contexts, using the method illustrated in Table V. Of the twenty-eight pairs, fifteen showed more aggression (as opposed to approachretreat interactions) when competition over males was compared with behaviour in other social contexts. In six of the fifteen cases the difference was statistically significant, and no pairs showed significantly less aggression. In addition, twelve pairs showed more approachretreat (as opposed to aggressive) interactions when competition over lactating females was Table HI. The Relative Rates of Agonistic Belmviour in Different Age-Sex Classes of Adult Baboons

Approachretreat interactions

Interactions involving aggressive behaviour

0.97

0.57

16 male-female dyads

1.21

0"13

28 female-female dyads

1.21

0.05

1 male-male dyad

Figures represent the mean number of interactions per hour per dyad, based on 90 hr of focal animal sampling on all possible dyads over a 15-month period. Each dyad had at least three interactions of both types. Table IV. The Relative Frequencies of Approach-Retreat and Actively Aggressive Interactions Between Females in Different Social Contexts. Based on Focal Animal Plus Sequence Sampling

Approachretreat interactions

Interactions involving active aggression

1051

486

infants lactating females

171 197 133

185 89 12

Interactions observed in other social contexts

550

200

pregnant N = 17 dyads

....

N=

lactating

dyads N =9dyads 6 decrease 9 no change 1 increase 2 no change Fig. 3. Changes in the rate of aggression related to the arrival of infants in seventeen female-female dyads. Increases and decreases in the rate of aggression are defined in[the text. Solid lines represent changes in the rate of aggression in at least some pairs; broken lines represent no observed changes.

Total interactions observed Interactions observed as competition for: adult males

SEYFARTH: SOCIAL RELATIONSHIPS IN FEMALE BABOONS compared with behaviour in other social contexts. In four of the twelve cases the difference was statistically significant, and no pairs showed significantly fewer approach-retreat interactions. Taken together, these results suggest that irt a number of dyads the social context of agonistic interactions affected whether females exchanged approach-retreat interactions or engaged in active aggression. They further suggest that females in general may have regulated their behaviour according to the 'objects' for which they were competing. Changes in the context of agonistic interactions over time. (i) Interactions over adult males. Females competed for access to adult males throughout the entire reproductive cycle. There was no indication that competition over males occurred relatively more often between females in one reproductive state than between females in another.

E. Tile Quality of Agonistic Behaviour In a number of primate species, agonistic interactions are known to be followed by 'friendly' behaviour between the individuals i n v o l v e d . Touching, kissing and grooming frequently follow aggression in chimpanzees (Van Lawick-Goodall 1968a, b; Nishida 1970), rhesus macaques (Sade 1965; Lindburg 1973), and captive stump-tailed macaques (BlurtonJones & Trollope 1968), while Blurton-Jones & Trollope also report that individuals tended to present when threatened. In the present study, both types of agonistic interaction were occasionally followed by proximity, presenting, or friendly behaviour between the individuals involved. Interactions where one of these occurred were considered to have been qualitatively different from interactions

1~176

(ii) Interactions over infants and lactating females. Figure 4 shows that agonistic interactions over infants were most frequent when the infants were youngest, and Fig. 5 shows that this was also true for competition over access to lactating females. These data, as well as those presented earlier (Fig. 1), suggest that infants were most attractive to others when they were youngest, and that both their attractiveness and that of their mothers declined with increasing infant age. Table V. The Method Used to Determine Whether Social Context Affected the Type of Agonistic Interaction Between Females

Over access to adult males

Other social contexts

Approach-retreat interactions

A

B

Aggressiveinteractions

C

923

t

-..._ 026 7-'10 11514 15-18 19-22 INFANT AGE (WKS.)

Fig. 4. The number of agonistic interactions between females over access to an infant at various infant ages. Solid line = approach-retreat interactions, broken line = interactions involving active aggression. N = 7 infants, eight adult females. Based on focal animal plus sequence sampling.

U3

z 60-

D ou

A, B, C and D represent four different combinations of agonistic behaviour and social context. All twenty-eight possible dyads were tested in the manner illustrated. In addition to interactions over adult males, interactions over access to infants and lactating females were also compared with behaviour in all other social contexts (see tex0. Competitive interactions between females did not occur in quick succession, thus data for any dyad are independent of each other. ~ 2 tests were used where the expected probability in each cell was greater than or equal to five, Fisher Exact Probability Tests were used in all other cases. Two-tailed region of rejection, P ~<0"05.

zw

~zm0'--6 7'-10 11:14 15'-18 19-22 tNFAN T AGE (WKS.)

Fig. 5. The number of female-female agonistic interactions over access to a lactating female at various infant ages. Legend as in Fig. 4.

924

ANIMAL

BEHAVIOUR,

where none occurred and the partners simply separated. The time interval between agonistic interactions and subsequent proximity or affiliative behaviour. Regardless of the sampling method in use

/

4

(see above) when an agonistic interaction between females was observed the individuals were followed for 15 min to see whether subsequent proximity (tolerance within 3 m) or affiliative behaviour occurred. As Fig. 6 illustrates, when proximity or affiliative behaviour did occur they most frequently followed within one minute. Approach-retreat interactions were followed .:by such behaviour proportionately more often than were interactions involving aggression. Changes in the quality of interactions related to changes in reproductive state.

N=466

N=I0~I

24,

~c

(i) Changes in the fi'equency of subsequent proximity or a~liative behaviour. As with other <1

1

5

15

5

1


MINUTE5

!5

LATER

Fig. 6. The time interval between female-female agonistie interactions and any subsequent proximity or affiliative behaviour. Graphs show approach-retreat interactions (N = 1051) and interactions involving active aggression (N ---- 486). Solid line = subsequent proximity, broken line = subsequent affdiative behaviour. Based on focal animal plus sequence sampling.

Both Q Q ~ pregnant N = 17 dyads

One Q t a c t . BothQQ ~ . ---~-lactating Proportionately more Proximit~ A.ffiL beh. Both 8

10

7

2

1

1

o

o 0

Significantly more Proximity_ AffiL beh. Both 8

7

. 6

One Q lact. BothQ Q Both Q 9 ........ One ~ . . . . . lactatin~ pregnant P r o ~ n a t e l y more N = 17 dyads Proximity AffiL bah. Both 8

10

6

1

1 0

0

0

Signih"lcantly more Proxlmit~ Affil. beh. Both 5

4

4

0

Fig. 7. Changes in the quality of agonistic interactions

related to the arrival of infants in seventeen femalefemale dyads. Upper diagram illustrates changes in the quality of approach-retreat interactions, lower diagram considers interactions involving aggressive behaviour. All seventeen possible dyads were tested against themselves from one condition to the next, using x2 or Fisher tests. Significantdifferenceswere those in which the twotailed P ~<0.05. No dyads showed proportionately less proximity or affiliativebehaviour.

measures of agonistic behaviour between females the quality o f interactions was mmffected by whether there were two sexually cycling females, one cycling and one pregnant female, or two pregnant females in any dyad. Significant changes did occur, however, when either one or both females were lactating. As noted above (Fig. 3), seventeen dyads were observed to make the transition from 'both females pregnant' to 'both lactating'. Data in Fig. 7 show that, i r t a large proportion of these dyads, the arrival of one infant resulted in either a relative or a significant increase in the proportion of agonistic interactions which were followed by proximity, affiliative behaviour, or both. When a dyad progressed from having one lactating female to having two, however, few further changes in the quality of agonistic interactions were observed.

(ii) Changes #1 the initiation of affiliative behaviour. The arrival of infants also produced changes in the initiation of afftliative behaviour following agonistic interactions. Data in Fig. 8 show that, when neither female in a pair was lactating, subordinate were generally more responsible than dominant individuals for the initiation of affiliative behaviour after bouts of aggression. After approach-retreat interactions both the dominant and the subordinate were equally likely to do so. In contrast, when one female in a dyad was lactating and the other was pregnant or sexually cycling, t h e :lactating female tended to receive more affiliative be, haviour regardless of her relative status. F. Coalitions Coalitions occur whert one animal joins another in aggressive action against a third. In a study of coalitions among gelada baboons, Bramblett (1970) suggested that coalitions

SEYFARTH: SOCIAL RELATIONSHIPS IN FEMALE BABOONS a m o n g adult females were more likely to- occur between individuals of similar rank, while

observers of both rhesus and Japanese macaques suggest that adult female coalitions are most eomrnonly formed between blood relatives, who also occupy adjacent positions in the dominance hierarchy (Koyama 1967; Sade 1967). In this study, coalitions among adult females were relatively rare. On thirty-two occasions one female was observed to join another in aggressive action against a third animal. Coalitions did not appear to have been formed against particular individuals, nor were specific individuals noticeably more active than others in forming coalitions. Though based on a small sample, data in Table VI show that seven of eight adult females formed coalitions with their 'nearest neighbours' in the dominance hierarchy (i.e. females o f adjacent rank) more often than would have been expected. Within each nearest neighbour dyad, however, there was no relation 50" (~)

',

~5

between the relative ranks o f the two individuals and the relative frequencies with which each formed coalitions with the other. G. Summary: Agonistic Behaviour (1) Females could b e r a n k e d in a stable, linear hierarchy which accurately predicted the direction o f most agonistic interactions. R a n k order did not predict which females would be most aggressive, nor did it predict which pairs o f individuals would exchange aggression most frequently. (2) Females with adjacent ranks in the hierarchy did, however, have agonistic interactions which differed from those in other dyads, since they were more likely t h a n others to form coalitions during aggressive interactions. (3) Over half o f all agonistic interactions between females were related to competition for access t o either adult males, infants, or lactating females. Individuals appeared to use different 'aggressive strategies' depending o n the social context. Females competed for eccess to adult males t h r o u g h o u t their reproductive cycles, while competition for access to infants or lactating females was greatest w h e n the infants involved were youngest. Table VI. The Distribution of Coalitions Among Females

t/~

"

I-- 1G

"

g

-

laJ I-7

"-

, m

kl_ 9

0

INITIATED BY [] DOM]

(b)

Z :

N N ",,4 N N

NEITHER

Q

LACT.

MOTHER "DOM. SUB. ONE Q LACT.

BOTH QQ LACT.

Fig. 8. The initiation of affiliative behaviour following (a) approach-retreat interactions, and (b) active aggression between females in different reproductive states. Based on focal animal plus sequence sampling.

Proportion of coalitions formed with nearest neighbours (,%) Females

Expected

Observed

N

H

14"3

60.0

5

Wel.

28 "6

83.3

6

Lys.

28.6

66"7

3

Shir.

28 "6

50"0

6

LP

28.6

66-7

3

PM

28 '6

33"3

6

M

28 -6

50'0

2

Patch

14.3

0.0

1

Sign Test, two-taiied, P = 0-07. -Expected values represents the proportion .of each female's coalitions which she might have been expected to form with her nearest neighbour(s) under the null hypothesis that coalitions are formed randomly among all individuals. Note that the highest- and lowest-ranking females have lower expected values because they have only one nearest neighbour, Observed values based on focal animal plus sequence Sampling.

926

ANIMAL

BEHAVIOUR,

24,

4

Animals to whom presents are directed may occasionally respond by mounting, touching, hugging or kissing the presenting animal (Blurton-Jones & Trollope 1968; Van LawickGoodall 1968a; Saayman 1972; Hausfater 1975). In the following section, only presents which occurred in non-agonistic social contexts are considered. Presents which occurred in the context o f agonistic interactions were considered in section I, E above. In addition, data on the frequency of response (see above) to each female's presents are taken as one measure of her 'attractiveness' to others at the time of presenting. This measure of attractiveness is analogous to that used by laboratory workers in studies where the response to presents was almost invariably mounting (e.g. Michael 1968; Herbert 1970). Frequency of presenting was related to an individual's status (Table VII). High-ranking females presented less often, and received more presents, than other individuals. There was no indication that the frequency of presenting varied with changes in reproductive state. The effectiveness of presents, or the frequency with which they received any of the responses listed above, varied with the reproductive state of the presenting female. Data in Table VIII show that females generally received the most frequent responses to their presents during

(4) In all dyadic relationships, significant changes in the frequency and quality of agonistic interactions occurred whenever either individual gave birth, while other changes in female reproductive state (i.e. within the sexual cycle or from sexual cycling to pregnancy) had no apparent effect on agonistic behaviour. When behaviour durmg lactation was compared with that at other tim.es, (a) lactating females received many more m e n d l y approaches, and avoided these approaches depending on the age of their infants and regardless of the rank of the approacher. ( b ) Dyads with one or two lactating females generally had a lower frequency of active aggression than others. A decrease in the frequency o f aggression was equally likely whenever either the dominant or the subordinate female gave birth. (c) Dyads with one or two lactating females were more likely than other dyads to follow both types of agonistic behaviour with either proximity or afliliative interaction. Results: H. Afliliative Behaviour

A. Presents Presenting (orienting the rump toward the face of another) occurs in many species of primates, and is generally thought to contain motivational elements of submission or conciliation on the part o f the presenter (Rowell 1972).

Table VII. The Frequency of Presents by Eight Adult Females Over a 15-month Period, and Its Relation to Female Rank

Order

Presenting females

H

Wel.

Lys.

Shir.

Presentees LP PM

H

M 1

Wel.

20

Lys.

6

3

Shir.

33

16

4

LP

27

7

11

8

PM

20

1

7

2

4

M

24

9

12

12

5

16

Patch

15

13

14

14

10

10

5

145

49

48

3t

t0

Total presents received

Patch

Total .presents gtven 1

1

21 9

3

3 2

36 22 rs = 0"95, P < 0"01

1

60 r s = - 0 . 8 8

3

2

60

1

2

37 P < 0"01

5

83 81

11

Spearman COrrelations (rs) indicate the extent to which presenting and receiving presents were inversely and directly correlated with rank, respectively.Based on focal animal plus sequence sampling.

SEYFARTH: SOCIAL RELATIONSHIPS IN FEMALE BABOONS

927

Frequency of grooming solicitations was also affected by the particular individuals involved. All eight adult females solicited grooming from their nearest neighbours in the dominance hierarchy more often than would have been expected (Table IX). Within each relationship there was no relation between the relative ranks of the two individuals and the frequency with which each solicited grooming. Finally, although solicitations occurred most frequently between nearest neighbours, their rate of response to each other's solicitations was comparable to that for other pairs. There was some indication, however, that the effectiveness of a female's grooming solicitations was directly related to her rank. Data in Table X indicate that females were most likely to respond to the solicitations from high-ranking individuals; data thus suggest that both rank and reproductive state (see above) affected the attractiveness of art individual female to others. This point will be discussed further below.

lactation, supporting the idea that individuals were most attractive to others when they were rearing young infants (see above, Figs 1, 5 and 8). B. Grooming Solicitations

In a number of primate species, an individual may present by orienting its flank, rather than its rump, toward the face of another. Such gestures frequently elicit grooming from the other animal, and have been interpreted as 'grooming solicitations' in anubis and hamadryas baboons (Kummer 1968; Rowell 1972), rhesus macaques (Altmann 1962; Sade 1965), stumptailed macaques (Blurton-Jones & Trollope 1968), and chimpanzees (Van Lawick-Goodall 1968b). In the present study, analysis of data on grooming solicitations attempted to answer three questions: first, how was the rate of a female's grooming solicitations affected by changes in her reproductive state?; second, to whom did each female direct the majority of her solicitations?; and third, which females received the highest rates of response per solicitation 9. Seven of the eight adult females showed the highest rate of grooming solicitations during lactation (Fig. 9). This suggests that females may have been attempting to 'take advantage' of their increased attractiveness to others during lactation (see above) by increasing the rate of their requests for grooming. However, the rate of response to these solicitations was not highest during lactation (see below).

C. Friendly Gesttwes Data in sections I, E. and II, A. have already shown that females often gave touches, hugs or kisses to others after agonistic interactions or in response to presents. This section considers the distribution of friendly gestures in all other social contexts. Friendly gestures to lactating females. Studies of the frequency of touching, kissing and embracing among a number of adult female primates have shown that during lactation the

Table VIII. The Proportion of Each Female's Presents which Received Responses, and Her Reproductive State at the Time. Based on Focal Animal Plus Sequence Sampling

Sex cycling Females H

No. of presents 1

Pregnant

Response (%) 0

No. of presents .

Lactating

Response (%) .

.

No. of presents

Response (%)

.

Wel.

--

--

7

43

14

79

Lys.

5

0

2

50

2

50

Shir.

5

20

17

24

39

64

LP

20

20

10

20

30

67

PM

6

33

3

0

28

57

M

48

15

40

13

5

40

Patch

41

20

23

35

28

86

928

ANIMAL

BEHAVIOUR,

24,

4

9 E x . CYCLE -r

5'

[]

PREGNANCY

[]

LACTATION

I--

Z

{!. L FEMALES

.

"

tiN DESCENDING

L

.

.

.

PATCH.

RANK ORDER)

Fig. 9. Tlie rates at which individual females solicited grooming in different reproductive states. Based on focal animal plus seauei~ce sampling.

mother's attractiveness and the infant's attractiveness to others are closely related. Among rhesus monkeys, baboons, and vervet monkeys, infants are known to receive friendly gestures at the highest rate when they are youngest (Hinde, Rowell & Spencer-Booth 1964; Rowell, Din & Omar 1968; Spencer-Booth 1968; Struhsaker 1971), while among both baboons and patas monkeys mothers also receive friendly Table XI. the Distribution of Grooming Solicitations Among Females Proportion of grooming solicitations directed to nearest neighbours (%) Females

Expected

Observed

N

I-I

14.3

25-0

39

Wel.

28.6

43.0

48

Lys.

28-6

48"0

33

Shir.

28"6

51.0

52

LP

28.6

34"0

29

PM

28.6

48-0

32

M

28.6

46"0

39

Patch

14.3

19-0

26

Sign Test, two-tailed, P < 0.01. Expected values represent the proportion of each female's grooming solicitations which she might have been expected to direct to her nearest neighbour(s) in the hierarchy under the null hypothesis that grooming solicitations are distributed randomly among all individuals. Observed values based on focal animal plus sequence sampling.

gestures most often when their infants are youngest (Hall & Mayer 1967; Rowell, Din & Omar 1968; RoweU 1969). In the following sections I divide friendly gestures to mothers into two types, and show that their frequency varied in a manner similar to that described above.

'Appeasement' friendly gestures. Roughly three-quarters of the friendly gestures given to lactating females occurred when an individual was friendly to a mother immediately before, as, or after she was friendly to the mother's infant. For example, one female might approach a mother and infant, kiss the mother, then touch the infant. Two sorts of data support the observer's impression that in these contexts individuals were behaving as if they meant to ~appease' or 'reassure' a potentially anxious mother. First, appeasement gestures occurred most frequently when mothers were most anxious (compare Figs 10 and 2). Second, since highranking females received more submissive behaviour than others (Table I), it might be expected that individuals wot~ld have been more submissive when handling the infants of highranking females, and thus that high-ranking mothers would have received more appeasement gestures than low-ranking mothers. In fact, high rank was positively correlated with a high frequency of appeasement (rs = 0.73, P < 0.05), though only during the infants' first 6 weeks. Other friendly gestures to lactating females. A smaller number of friendly gestures to lactating females occurred when one animal simply approached a mother-infant pair artd hugged,

SEYFARTH: SOCIAL RELATIONSHIPS 1N FEMALE BABOONS

929

Table X. Ranked Frequendes with which Each Female Responded to the Grooming Solicitations of Others. The Relative Frequencies with which Each Female (Rows) Responded to the Grooming Solicitations of Others (Columns) are Ranked. Solicitors Responder

H

Wel.

Lys.

Shir.

LP

PM

M

Patch

3

1"5

1"5

4

5

6

7

4.5 1

--

4-5 3

1 4"5

3 4"5

6"5 7

6"5 6

2 2

3 2

1

7

4

6"~

6 5 4 5

H

--

We1. Lys,

2 2

Shir LP

4.5 2

PM

1-5

3

5

1"5

M 1.5 Patch 1 Sum ofranks 14.5

3 3 17

4 3 23

1.5 5 23

--

-

4"5 -7 7 6 34

-

6"5

80 t

i.

_m ff b 9 ~2C

--

6 7 30.5

6 --

3 42

- -

39-5

between individual females. Specifically, alt h o u g h females with adjacent ranks in the hierarchy h a d social bonds which were stronger and m o r e persistent than f o u n d in other pairs (see below), these females did not interact more frequently than others during lactation, n o r did mothers allow females o f a d j a c e n t rank greater access than others t o their infants. The later development o f individual adult female-infant preferences is discussed in Cheney Seyfarth (1976). Friendly gestures to sexually cycling or pregnant females. Twelve per cent o f all observed friendly gestures were given to females w h o were either pregnant or sexually cycling. These occurred, for example, when two females were foraging together and one approached and kissed the

O-6 7-9 ~5-~ 19'-22 INFANTAGE(WKS,) Fig. 10. The percentage of friendly gestures to infants which were accompanied by ~i friendly gesture to the infant's mother at various infant ages. N = 7 motherinfant pairs. Based on focal animal plus sequence sampling. touched or kissed only the mother. These gestures occurred most frequently when infants were youngest, and declined with increasing age thereafter (Fig. 11). Differences between dyads in the frequency of friendly gestures to lactating females. The freq u e n c y o f friendly gestures t o mothers and their infants were solely infant-age-dependent, and did not reflect the long-term social b o n d s .

n z w

o~

Z

0'-6 7-'10 11'-1415'-1819'-2223INFANTAGE (WKS.). Fig. 11. The frequency with which mothers received friendly gestures from other females during lactation, at various infant ages. N = 7 mothers through infant age 22 weeks, N = 5 mothers thereafter. Based on focal animal plus sequem~ sampling.

ANIMAL

930

BEI-IAVIOUR,

other. In this social context, seven of eight adult females directed more friendly gestures than would have been expected to their nearest neighbours in the dominance hierarchy (Table

XI). D. Grooming Frequency of grooming and changes in reproductive state. (i) Groomb,g and oestrus. Kummer & Kurt (1965) and Rowell (1968) found that oestrous females generally groomed less and received less grooming than females in other reproductive states. In the present study, no relation was found between grooming and changes either within the sexual cycle or from sexual cycling to pregnancy. However, an individual female generally did not groom others during her sexual consortships, which occurred for short periods during her swollen stage (Seyfarth, in preparation, a). (ii) Grooming and lactation. In a number of primate species, females receive more grooming during lactation than during either sexual cycling or pregnancy (Hall & Mayer 9 Rowell !968, 1969; Sugiyama 1971). Struhsaker (1971) has further shown that, among vervet monkeys, the amount of grooming received by lactating females declines with increasing infant Table XI. The Distribution of Friendly Gestures to Sexually Cycling or Pregnant Females Proportion of friendly gestures received from nearest neighbours (%) Females

Expected

Observed

N

I-I

14.3

66.7

9

Wel.

28.6

62.5

8

Lys.

28.6

57.1

7

Shir.

28.6

45.4

l1

LP

28.6

50.0

4

PM

28-6

,42.8

7

M

28.6

40-0

5

Patch

14.3

25.0

4

Sign Test, two-tailed, P < 0.01. Expected values represent the proportion of each female's friendly gestures which she might have been expected to receive when sexually cycling or pregnant from her nearest neighbour(s) in the hierarchy under the null hypothesis that friendly gestures are distributed randomly among all individuals. Observed values based on focal animal plus sequence sampling.

24,

4

age (see also DeVore 1963; Kaufmann 1966). In the present study, females not only received the most grooming (Fig. 12) but also were groomed by more different individuals (Fig. 13) during lactation than during other reproductive states. Two further points are important. First, unlike either friendly approaches or friendly gestures (Figs 1, 10 and 11), the amount of grooming received during lactation did not necessarily decline with increasing infant age, but varied in different ways for different females. Second, data in Fig. 13 also indicate that in all three reproductive states high-ranking females were groomed by more different individuals than 50,

d"-

~o SEXUAL PRG. 0'--6 7'-10 11:14 15:18 19'-22 23LACTATION: INFANT AGE (WKS.) CYCLE Fig. 12. The frequency with which individual females received grooming each month during sexual cycling, pregnancy, and, during lactation, at various infant ages. Based on 120 instantaneous samples each month on each female. N ~- 7 females through infant age 22 weeks, N = 5 females thereafter.

I sex. CYCLE

{L ~n ~J4-

j

~1 PREGNANCY E] LACTATION

O2J o

H

WEL. LYS. SH~. LP PM. M FEMALES (IN DESCENDINGRANKORDER)

PATE:H.

Fig. 13. The mean number of females who groomed each individual each month during sexual cycling, pregnancy~ and lactation. Based on instantaneous sampling. Correlations between rank and mean number of groomers are: during sexual cycling, rs -----0.46, NS; during pregnancy, rs = 0.65, P < 0.05; during lactation, rs = 0.81, P < 0.05.

SEYFARTH: SOCIAL RELATIONSHIPS IN FEMALE BABOONS were low-ranking females. This point is discussed further in the following section, Although all females received the most grooming during lactation, there was no indication that mothers were groomed for longer bouts than others. Frequency of grooming and status. Observers of adult female primates have frequently suggested that the amount of grooming received by art individual is positively correlated with her rank (Bernstein & Sharpe 1966; Hall 1967; Sade 1972; Oki & Maeda 1973; Rhine 1973). In each case, conclusions have stated either that the total amount of grooming received by each individual was positively correlated with her rank, or that in each dyadic relationship subordinate females tended to groom more often than dominant females. In contrast, Rowell (1966) found no such relation between grooming and status among captive female baboons, nor did observers in four other studies of freeranging and captive Old World Monkeys (Bernstein & Mason 1963; Rosenblum, Kaufman & Stynes 1966; Bernstein 1970; Lindburg 1973). Lindburg's observations were made primarily during the birth season, which may have affected the pattern of female-female grooming (see above), while conclusions in the latter three studies were based on grooming among subadult and adult males and females, without correcting for possible age/sex differences in behaviour. In the present study, the following data suggest that there was a direct relation between high rank and the anlount of grooming received by each female. First, as noted above, changes in reproductive state had an important effect on the frequency of grooming between females. Taking this into account, in Table XII the amount of grooming received per month for individuals is compared separately during lactation and in other reproductive states. In both cases, the amount of grooming received was significantly correlated with rank. Second, data in Fig. 13 have already shown that in all reproductive states high-ranking females were groomed by more different individuals than were lowranking females. Third, the relative contributions of subordinate and dominant individuals to grooming ,in each dyad were compared when neither female was lactating (see below). In eighteen Of twenty-six dyads where grooming occurred, dominant individuals received more grooming than subordinates. Dominant individuals received less grooming in six dyads.

931

With one or two lactating females, grooming in each dyad followed this pattern less strictly, being affected by both the presence and the relative age(s) of the infant(s) involved. Although high-ranking females received more grooming than others, there was no relation between rank and the bout length of grooming received by each female. Grooming

and individual preference.

In

a

number of primate species, adult females in linear dominance hierarchies are known to groom animals whose ranks are similar to their own more than they groom others. This has been shown both in studies where the blood relations of individuals were unknown (Bramblett 1970; Lindburg 1971; see also Rhine & Kronenwetter 1972) and in studies where individuals of similar rank were known to be related by common descent (Kawai 1958; Sade 1965, 1967; Koyama 1967; Oki & Maeda 1973). If each individual grooms animals next to herself in the hierarchy more than she grooms others, and if she grooms animals increasingly less as their ranks become different from her own (see, for example, Lindburg 1973; Oki & Maeda 1973), the pattern of individual grooming preference may be described as follows: when a female grooms animals below herself in the Table XIL The Relation Between Rank and the Amount of Grooming Received by Each Female. Figures Represent the Mean Number of Instantaneous Samples Per Month when Each Female Was Being Groomed, in Different Reproductive States. During Lactation, All Individuals Observed For at Least 22 Weeks

Meanno. of instantaneoussamplesper month During sexual cycling Females and pregnancy

During lactation

H

6"7

20.4

Wel.

4.3

18.3

Lys.

6-6

29.4

Shir.

6-9 rs = 0.64

19"3 rs = 0"81

LP

4.7

15.5

PM

5.6

15.1

M

4.1

8.4

Patch

3.8

9.1

P < 0-05

P < 0"05

ANIMAL

932

BEHAVIOUR,

hierarchy she grooms them in direct relation to their status. When she grooms animals above herself in the hierarchy she grooms:them irt inverse relation to their status. Data in Figs 14 and 15 show that thiswas the pattern of grooming among adult female baboons in this study. Two points are important. First, data on grooming have been separated according to whether females receiving grooming were lactating or not (lactating, Fig. 14, not lactating, Fig. 15). In this way, preference for particular individuals, which remained relatively stable throughout the study, will not be confused with preference for females in particular reproduetive states, which fluctuated. Second, note that the three highest-ranking females showed similar preference patterns, with each tending

H 5 .

to groom all others in direct relation to their status. Each of the two lowest-ranking females tended to groom all others in inverse relation to their status. Further analysis suggests that grooming between nearest neighbours was also both more persistent regardless of changes in reproductive state and more reciprocal than grooming in other dyads. First, Fig. 16 considers the persistence of grooming throughout the 15-month study. Since each female gave birth to only one infant, and all were observed for approximately similar periods of lactation, grooming in all dyads was equally likely to have occurred because of the presence o f infants (see above). The persistence of grooming in all dyads is therefore compared directly, and nearest neighbour dyads are shown to have had grooming which was more persistent than that between other/individuals. Second, data in Fig. 17 indicate that grooming between nearest neighbours was more likely to be reciprocal than that between other individuals.

rs'~O0

o.

wL,

5t

;',.

t~

/

4

E. Summary: Affdiative Behaviour (1) The frequency of an individual's presents in non-agonistic social contexts was related to

L~P

~

24,

T I--

,s,oas"

%=o.a2"

r~,-080 i tP

i H

rs:-0.87

rs=~:O0

Z

~

;~,

~s"olo

WEL

r~: . 0 8 4 ~

r.s=.O.77'

~za ~OreERS Fig. 14. The relation between rank order and grooming preference among females. X-axis shows eight different groomers, arranged in rank order. Y-axis shows the mean number of instantaneous samples per month devoted tO grooming other females who were lactating (for the grooming of non-lactating females, see Fig. 15). Spearman correlations (rs) illustrate the extent to which each individual female groomed those below herself in the hierarchy in direct relation to their status, and groomed those above herself in the hierarchy in inverse relation to their status. * = P < 0.05. Further explanation in text.

i

M

L~

5t

~:-os7 GFEO~EF~S

Fig. 15. Legend as in Fig. 14, except illustrating the grooming of non-lactatingfemales.

SEYFARTH: SOCIAL RELATIONSHIPS IN FEMALE BABOONS

her status. High-ranking females presented less often, and received more presents, than others. The effectiveness of presents was related to the :reproductive state of the presenting female. Each female received the most frequent responses to her presents during lactation. (2) The frequency of grooming solicitations was related to both reproductive state and individual preference. Females generally solicited grooming at the highest rate during lactation, and in all reproductive states were most likely to solicit from animals next to themselves in the dominance hierarchy. The effectiveness of grooming solicitations was related to status. High-ranking females were more likely than lowranking females to have successful grooming solicitations. (3) Over 80 per cent of all friendly gestures were given to lactating females. During lactation, females received friendly gestures most often when their infants were youngest. The frequency of friendly gestures to lactating females was related both to the attractiveness of mother and infant at various infant ages and to attempts by others to 'appease' mothers while gaining access to their infants. Individuals with adjacent ranks in the hierarchy were significantly more ~likely than others to continue friendly gestures during sexual cycling and pregnancy. (4) During lactation, all females both received more grooming and were groomed by more different individuals than when either sexually

933

cycling or pregnant. In all reproductive states, high-ranking females received more grooming and were groomed by more different individuals, than others. When differences in grooming due to changes in reproductive state were held constant, individuals appeared to groom animals next t o themselves in the hierarchy more than they groomed others. Discussion The distribution of afliliative behaviour among the adult females in this study may be summarized in terms of their dominance relations and two principles governing the attractiveness of individuals to others: (1) All females are most attractive to others when they are lactating (Figs 1, 5, 8, 10, 11, 12, 13; Table VIII). (2) In all reproductive states, high-ranking females are more attractive than lowranking females (Fig. 13; Tables X, XII). 'Attractive' females are defined as those who receive the most friendly gestures (e.g. principle 1), the most grooming (principles 1 and 2), are groomed by the greatest number of individuals (principles 1 and 2), etc. Not investigated in this study, but clearly also of importance, are principles governing the attraction between members of the same genealogy (Sade 1965, 1972, see also the discussion below). 10'

0uq 7-

I---

Z O 9LL 10-

S/D

I

d Z

N=7

I

IN=21

Fig. 16. The persistence of grooming in different femalefemale dyads. Graph illustrates the number of months (mean and range) in which at least some grooming occurred, 'Nearest neighbour' dyads (N -- 7) are compared with all others.

5"

N=7

N=21 PAIRS

Fig. 17. The extent to which grooming was reciprocal in different female--female dyads. Graph illustrates

mean and range values for the ratio of grooming by the subordinate (S) to grooming by the dominant (D) in each dyad throughout the study. Nearest neigl?bour dyads are compared with all others. Since grooming is most reciprocal in those pairs whose ratio (S/D) is closest to 1"0,data suggestthat groomingbetweennearest neighbours was more likely to be reciprocal than that in other pairs.

ANIMAL

934

BEHAVIOUR,

24,

4

Middle-ranking females, however, will be affected by competition in the following way. When female D, for example (Table XIII), grooms females E, F, G or H, she is unlikely to receive competition from females A, B and C, who could limit D's access if they chose. This is because A, B and C all have great access to a number of individuals, and each has at least three females of higher rank (i.e. more attractive) than E, F, G or H among whom to distribute her grooming. Thus, meeting relatively little competition, female D will groom individuals beneath herself in the hierarchy in direct relation to their ranks, or attractiveness. However, when female D attempts to groom females A, B or C, her access to each will depend on the behaviour of the other two. For example, D will not be able to groom A when A is either grooming or being groomed by B or C, and when D finally does gain access to A she will be supplanted every time B or C approaches. Using the hypothetical data in Table XIII, it is possible to quantify the relative amounts of competition which female D will meet when attempting to groom either A, B, or C (Fig. 18(a)). The model suggests that female D will be able to groom animals ranking above herself in the hierarchy in inverse relation to their attractiveness, or

The Distribution of Grooming Among Females

Principle 2 appears at first directly to contradict the data presented earlier on the distribution of grooming a m o n g individuals in this study. Specifically, if high-ranking females are most attractive to all others, why did each female direct most of her grooming to the individuals ranking next to herself in the hierarchy (Figs 14 and 15)? The contradiction may be resolved by considering the interaction between rankrelated attractiveness and dominance among females. First, assume that all females are attempting to regulate their behaviour according to principle 2; that is, they are attempting to distribute their grooming in direct relation to the rank o f other individuals. Second, assume that there is no competition a m o n g females for access to each other. Each female will then be expected to distribute her grooming according to the attractiveness (or rank) of others, as illustrated in Table XIII. Where competition a m o n g females occurs, as it does in the natural situation, it will seldom act to restrict the behaviour of a high-ranking female. The grooming of high-ranking females will therefore continue to resemble that illustrated in Table XIII.

Table XIII. A Theoretical Distribltion of Grooming Among Females

Receivers Groomers

A

A

B

C

D

E

F

G

H

Total

25

21

18

14

11

7

4

I00

21

17

14

10

7

3

100

17

13

10

7

3

100

13

10

6

3

100

9

6

3

100

6

3

100

3

100

B

28

C

27

23

D

26

23

19

E

25

22

19

16

F

24

21

18

15

12

G

23

20

17

14

12

9

H

22

20

17

14

11

9

6

175

154

132

111

89

68

45

Total

100 22

The distribution assumes, first, that female attractiveness is positively correlated with rank, declining in a linear manner, and second, that there is no competition among females for access to each other. The values in each cell are calculated as follows, for example, cell A B : attr.B AB =

•

attr.a § attr.c § attr.D § attr.~ -t- attr.F + attr.o § attr.n

100

SEYFARTH: SOCIAL RELATIONSHIPS IN F E M A L E BABOONS

ranks. A similar argument may be applied to the lowest-ranking female, H, who will receive the most competition for access to female A and the least competition for access to female G (Fig. 18(b)). The model presented above resolves the apparent contradiction between behaviour according to the attractiveness of high-ranking individuals and the frequent grooming observed between females of adjacent rank in this and other studies (e.g. Sade 1965, 1967, 1972). The model also offers an alternative, or complementary, explanation to that suggested by Sade 0965) for the causal factors affecting the distribution of grooming among adult female primates. Sade has suggested that grooming occurs most often between females of adjacent rank because these individuals are members of the same genealogy, and thus share relations which have developed during infancy and persisted into adulthood. In contrast, the model presented here suggests that grooming occurs most often between females of adjacent rank because competition forces individuals to compromise their attraction to the highest-ranking females in the group. One of the reasons why it is important to distinguish between the two explanations above is that it would be of interest to know the extent to which natural selection may have favoured a 'behavioural strategy' by adult females based on their attraction to high-ranking individuals, or their attraction to members of their own genealogy, or both (see below). If females are attracted primarily to members of their own Ga~

~

200

Fig. 18. A theoretical representation of the amount of competition received by two females attempting to groom individuals who are higher-ranking than themselves. (a) Female D (see Table XIID will be unable to groom female A when A is either grooming or being groomed by femalesB or C. Using data from the hypothetical grooming distribution shown in Table XIII, the sum of cells ABq-AC-i-BA-t-CA equals D's competi-

tion for access to A. Similarcalculationsshow D's competition for access to femalesB and C. Co) Females H's competitionfor accessto all others.

935

genealogy (i.e. Sade's developmental explanation, above), then their behaviour may be interpreted at least partly in terms of kin selection (Hamilton 1964). In contrast, if females are attracted primarily to high-ranking individuals (i.e. the competitive model, above), then their behaviour is more accurately interpreted in terms of the benefits accruing to those animals who are able to form bonds with high-ranking adult females (e.g. Weisbard & Goy 1976). In conclusion, however, it seems most accurate to describe the affiliative behaviour of adult females in terms of both of the causal principles discussed above. By the time an individual female reaches adulthood, she will probably have developed preferences for her mother and sisters, and all are likely to occupy similar social ranks in the group (Koyama 1967; Sade 1967; Cheney Seyfarth, 1976). During adulthood frequent social interaction will reinforce bonds within the female's genealogy, and other factors may also make it unlikely that she will interact frequently with individuals whose ranks differ widely from her own. She will be less attracted to lower-ranking individuals than to her own relations, and though she may attempt to establish close bonds with animals of higher rank, her own status will limit her ability to do so. (Other discussions of the balance between attraction and competition in primate groups may be found in Crook 1970b, c; Rhine 1973; and Vaitl, in preparation). The Interaction Between Principles 1 and 2

Principle 1 (above) describes short-term changes in the attractiveness of individual females; principle 2 describes the attractiveness of individuals over a longer period. By considering the interaction between these two principles it is possible to suggest that changes in both dyadic relationships and social structure related to the arrival of infants will differ according to whether dominant or subordinate females give birth. When a female was lactating, changes in the frequency and quality of her interactions tended to make them more like the interactions of higher-ranking females. For example, lactating females received less aggression, more grooming, and more friendly gestures after agonistie interactions: all 'benefits' which usually accrued to the higher-ranking females in this group. It follows that changes in each dyadic relationship related to the arrival of infants will differ qualitatively depending on whether the

ANIMAL BEHAVIOUR,

936

relations (and thus social structure) therefore differed depending on the rank o f the female giving birth.

dominant or the subordinate female gives birth. If the dominant female gives birth, changes in the quality of interactions will tend merely to reinforce differences in status and attractiveness which already exist, whereas if the subordinate female gives birth such differences will become temporarily more ambiguous. Hinde (1976) has described primate social structure in terms of the patterning of relationships within each group. Using data on grooming from the present study, it is possible to show how the birth of an infant to a low-ranking female had a greater effect on female social structure than did the birth of an infant to a high-ranking female. In Fig. 19 two females are used as examples: Wellesley, ranked second, and PM, ranked sixth. Note that Wellesley, who was high-ranking and thus attractive to other animals (see above), received most of her grooming from other high-ranking females before her infant was born; after birth there was little change. In contrast, PM, who was low-ranking and thus less attractive to others, received very little grooming from high-ranking females before her infant was born but much more afterwards. Changes in the network of grooming

Acknowledgments For their assistance during field research I thank A. Botamani, S. Jacobs, M. Kilani, W. Mazwayi, W. Mazwayi, W. Prinsloo, a n d especially B. L. Penzhorn. I am grateful to Graham Saayman for both advice and hospitality throughout all stages of field research. In Cambridge I thank Les Barden, who photographed the drawings, and Pat Bateson, John Crook, Sandy Harcourt, and Michael Simpson, who read and criticized early drafts of this paper. I thank Joan Stevenson-Hinde for help with statistics, and Dorothy Cheney Seyfarth for insightful criticism throughout. Finally, I would like to express particular thanks to my supervisor, Robert Hinde, for his encouragement and criticism throughout all stages of this research project. 9 REFERENCES Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227-267.

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Fig. 19. Changes in the distribution of grooming received by two females during the first 10 weeks of lactation. (a) and (b) illustrate the distribution of groomingreceived by females Wellesley(ranked second) and PM (ranked sixth) throughout the 15-month study. (c) and (d) illustrate the distribution of grooming received by each femaleduring the first 10 weeks of lactation. Based on instantaneoussampling.

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(Received 14 November 1975; revised 23 February 1976; MS. number: 1488)