Changes in the dominance rank and reproductive behaviour of male bonnet macaques (Macaca radiata)

Anim. Behav., 1984, 32, 994-1003

CHANGES IN THE DOMINANCE RANK AND REPRODUCTIVE BEHAVIOUR OF MALE BONNET MACAQUES (MACACA RADIATA) BY AMY SAMUELS* w JOAN B. SILK~ w & PETER S. RODMAN++

*Ecology Graduate Group, University of California, Davis, CA 95616, U.S.A. "~AlleeLaboratory of Animal Behavior, University of Chicago, 940 E. 57th St., Chicago, IL 60637, U.S.A. +Department of Anthropology, University of California, Davis, CA 95616, U.S.A. Abstract. The dominance rank of male bonnet macaques influenced their associations and sexual interactions with cycling and conceiving females. Only high-ranking males formed exclusive associations with high-ranking females, and high-ranking males copulated with these females more often than did other males. Changes in male dominance rank were directly related to changes in male mating behaviour, as males who rose in rank spent increasing amounts of time in exclusive proximity to conceiving high-ranking females, and males whose ranks declined spent decreasing amounts of time in proximity to such females. The year of the study in which dominance relationships were most stable was also the year in which the top-ranking male most successfully monopolized access to conceiving high-ranking females. Among the major issues addressed by students of animal behaviour and evolutionary biology in the last decade have been (1) the relationship between social behaviour, adaptation and genetic fitness, and (2) the measurement and importance of dominance relationships among the members of social groups. It is therefore not surprising that there has been considerable interest in the hypothesis that male dominance rank is positively correlated with male fitness, and speculation about the origin and adaptive significance of this relationship. A large body of evidence has been accumulated in an attempt to evaluate the empirical relationship between dominance, reproductive success and genetic fitness. Dewsbury's (1982) detailed review of these studies indicates that despite a number of problenas associated with the collection, interpretation and statistical analysis of these data, there is substantive evidence that male dominance rank is positively associated with male fitness in several taxonomic groups, including primates, rodents, pinnipeds and artiodactyls. The form and nature of dominance relationships among males appear to vary considerably both within and between species, as do the behavioural strategies by which high-ranking males achieve reproductive success. These differences have largely precluded efforts to identify and compare ecological and social

factors that influence the relationship between dominance rank and reproductive behaviour. In this paper we describe some aspects of the relationship between male dominance rank and reproductive behaviour in a large multi-male group of bonnet macaques (Macaea radiata). In particular, we describe substantial changes in the male dominance hierarchy which occurred over a 3-year period, and document corresponding changes in patterns of association and sexual interactions between males and conceiving females. These data suggest that several dimensions of male dominance relationships may influence the relationship between male dominance rank and reproductive success.

Subjects and Methods A. History, Composition, and Management of the Study Group In October 1970, 76 bonnet macaques were placed in a 0.2-ha outdoor enclosure at the California Primate Research Center (CPRC) at the University of California, Davis. In July 1971, 23 juveniles were added to the group to replace monkeys that died or were removed from the group during the previous winter. The resultant group was composed of wild- and captive-born monkeys of all age and sex classes. This group has been maintained intact for behavioural research since 1975. All demographic changes in the group after 1975 were due to births, deaths, and removals of individuals with serious health problems. Table I (adapted from Silk et al. 1981a) details changes in the composition of the group during the 3-year study period.

w

addresses: A. Samuels: AUee Laboratory of Animal Behavior, University of Chicago, 940 E. 57th St., Chicago, IL 60637, U.S.A. J. B. Silk: California Primate Research Center, University of California, Davis, CA 95616, U.S.A. 994

SAMUELS ET AL.: CHANGES IN RANK AND MATING

995

Table I. Demographic Composition of the Group (October 1, 1977-October 1, 1980)

Class Adult male Adult female Subadult male Juvenile male Juvenile female Infant male Infant female Infant unknown sex Total

Age (years/months) >7.0 >3.6 5.0-6.11 1.0-4.11 2.0-3.6 <1.0 < 1.0 < 1.0

1977

1978

1979

1980

5 28 3 15 4 7 (12") 4 (11) 0 (1) 66

6 29 2 19 4 5 (15) 6 (5) 0 72

7 30 4 16 6 6 (8) 4 (11) 0 (2) 73

8 28 6 19 7 4 7 ! 80

*Number of infants born in the group in parentheses. H u m a n intervention is limited to daily feeding and health surveillance of the animals, and occasional maintenance work done in and around the enclosure. Seriously ill or injured animals are hospitalized, treated and returned to the enclosure upon recovery. Three times each year, all the animals in the group are captured, dyemarked for individual identification, and given physical examinations. All behavioural observations are conducted from outside the enclosure. Wooden A-frame structures, concrete culverts and covered perches provide shelter for the monkeys in the 30.5 x 61-m chain-link enclosure. In addition, there are swings, stationary oil drums, large logs and a climbing structure in the enclosure. Commercial monkey chow and water are available ad libitum. The monkeys also forage extensively on grass, the predominant ground cover. B. Data Collection This analysis is based upon data that were collected between October 1977 and August 1980 during 1629 h of focal-animal observations and 68 h of point samples of adult females, adult males and subadult males (sampling terms defined by Altmann 1974). Different types of information about the associations of males and females were obtained during the 3-year study period. During focal-animal sampling each subject was observed for at least two 20-min periods each week. The identities of certain animals (targets) within 3 m of the focal subject were recorded at 30-s intervals. The identity of the animal responsible for initiation ('approach') and termination ('leave') of each bout of proximity, and details of sexual and agonistic interactions involving the focal animals, were recorded continuously. In addition, details of sexual and agonistic interactions involving indi-

viduals other than the focal subject were recorded ad libitum. During point sampling, each subject was observed at least 36 times per week. The identities of all animals within 3 m of the subject at a specified instant were recorded. Point samples collected during the conception periods of focal females were used to verify the patterns that emerged from the analysis of the limited number of focal observations of conceiving females collected during the first year of the study. In this report we focus upon male rank relationships and mating behaviour during the three breeding seasons of the study period. The breeding season was defined as the period of time between the conceptions of the first and last full-term infants born in each year, and was identified retrospectively. C. Subjects All males who were at least 6 years old in September of a given year became subjects of focal observations during that breeding season. Male 15 (M15) was added to the sample in 1978, and male 79 (M79) was added to the sample in 1979. The oldest male in the group, M99, was born in the wild some time before 1966. All other males were born in captivity (M22 and M24 in 1969, M29 and M32 in 1970, M61 in 1971, M15 in 1972, and M79 in 1973). Female subjects ranged in age f r o m 5 to approximately 12 years at the beginning of the study (mean a g e = 8 years). All but the oldest female, female 21 (F21), were born in captivity, and all focal females were multiparous at the beginning of the study. D. Determination of Dominance Rank Focal and ad libitum observations of aggressive and submissive behaviour directed by one

996

ANIMAL

BEHAVIOUR,

individual toward another individual were used to assess dominance ranks. When one animal directed an aggressive act (e.g. shove, hit, chase, bite, attack, forcible displacement) toward another individual, the actor was considered to be the dominant interactant. The recipient of an aggressive act or the initiator of a submissive act (e.g. screech, grimace, crouch, flee) was considered to be the subordinate interactant. Polyadic interactions were excluded from analysis, as were dyadic interactions in which the outcome was unclear. Undecided interactions include encounters in which the same individual performed both aggressive and submissive behaviours, and encounters in which both individuals performed aggressive or submissive behaviours. Ordinal dominance ranks were assigned to the 29 adult females in the group (Silk et al. 1981b). The dominance hierarchy was constructed so as to minimize the number of entries below the diagonal of the dominance matrix (reversals). Only minor changes in female rank relations occurred during the 3-year study period (Silk 1982). The sample of focal females included the highestand lowest-ranking females in the group in 1978 ( F 3 4 = r a n k 1, F 4 7 = r a n k 5, FI1 = r a n k 7, F21 = rank 9, F38 = rank 12, F37 = rank 21, F12 = rank 23, F 4 4 = r a n k 27, F41 = r a n k 28, F19 = r a n k 29). Females drawn from the top and bottom halves of the dominance hierarchy are referred to as high-ranking and low-ranking females, respectively. The same procedure was used to calculate the ordinal dominance ranks of males during the breeding seasons of the second and third years of the study. The ordinal rank order of males during the 1977 breeding season was obtained from Glick (1980), who studied this group of bonnet macaques from 1977 to 1978. Her data are consistent with our more limited ad libitum observations of male dominance interactions during the same year. Boyd & Silk (1983) have developed a statistical method that uses information from a dominance matrix to generate a cardinal index of dominance rank for each individual. These indices provide an estimate of the 'amount' by which one individual dominates another, and allows the significance of the differences in rank among the members of any set of individuals to be assessed. The cardinal indices of dominance rank were computed for males from data collected during the second and third years of the study (Fig. 1). Two rank orders are presented for the 1978

32,

4

breeding season, because a major change in the dominance hierarchy occurred during that period. Because comparable data were not available for the first year of the study, cardinal indexes could not be computed for 1977. The ordinal and cardinal dominance rank orders of males are nearly identical. Where discrepancies do occur, the cardinal dominance indices of the males in question are very similar. Males were ranked according to their cardinal indices. The resultant cardinal rank order was used to evaluate the relationship between male dominance rank and behaviour in 1978 and 1979, and the ordinal rank order was used to evaluate the relationship bet1977

C;~ [ 99

1978A

d L.e9

29

61

5.2

22

24

61

5.2

29

22 (7_9) (24)

2~ ~5

(IS) (79)

1 .6G .

1978B

0

9.64

1979

Fig. t. Cardinal dominance indices of males. In each time period, males are listed by identification number in decreasing rank order. The heights of the bars correspond to the values of the cardinal indices of dominance rank, which are given in the lower portion of each bar. The identification numbers of young males who were not focal subjects are enclosed in parentheses. A solid line connecting two bars denotes a rise in rank from one time period to the next; a dotted line denotes a fall in rank. The 1977 rank order is based on ordinal ranks (see text for explanation). It was not possible to calculate a cardinal index for M24 in 1978A because he never challenged another male. M48 ranked between M24 and M15 in 1977, but died early in the 1977 breeding season.

SAMUELS ET AL.: CHANGES IN RANK AND MATING ween male dominance rank and behaviour in 1977. E. Identification of the Conception Periods of Females Female bonnet macaques do not exhibit morphological or behavioural signs of ovulation that are discernible by human observers (Parkin & Hendrickx 1975). We were able to identify ovulatory cycles that resulted in the conception of a full-term infant retrospectively, by counting back 165 days from the infant's birthdate (gestation=165 days; Hendrickx & Binkerd 1979). We were not able to identify other periods of sexual receptivity. Because the gestation lengths of female macaques are reported to be quite variable (MacDonald 1971 ; Stabenfeldt & Hendrickx 1972; Bielert et al. 1976; Nigi 1976), the period of probable conception was defined as an 11-day period which began 5 days before and ended 5 days after the probable date of conception. Focal observations of each female and all males were conducted on an average of 7.5 days during each female's conception period (range = 5-10 days). F. Terminology A consort relationship is usually considered to be a prolonged and continuous association between a male and a receptive female (e.g. Hausfater 1975). Because we did not sample males and conceiving females continuously, we cannot accurately assess the duration or continuity of associations between males and conceiving females. In the absence of this information, we have used other terms to describe associations between males and females. The number of intervals in which only one male was in proximity to a focal female during her conception period was determined for each female. Conception periods of the same female in different years were treated separately in the analysis. The male responsible for the largest number of intervals of exclusive proximity to a given female in a given breeding season is referred to as the female's 'most common companion'. If a male was in exclusive proximity to a focal female significantly more often than were all other males combined, he was considered to be her 'primary companion'. T h e normal approximation of the binomial test was used to assess the significance of this difference. Results The analysis of the relationship between male dominance rank and mating behaviour is corn-

997

plicated by the fact that the male dominance hierarchy changed substantially during the course of the study period. These changes are described in some detail below. Since the rank order and stability of the male dominance hierarchy were different during each year, the behaviour of males during each breeding season was analysed separately. A. Changes in Male Dominance Rank M99 had been the top-ranking male in the group since 1973 (Judge & Rodman 1976; Simpson 1976), and was rarely challenged by other males between August 1977 and August 1978 (Glick, unpublished data; Samuels & Silk, unpublished data), the first year of our study. By the beginning of the 1978 breeding season, however, several changes in the male dominance hierarchy had occurred. M15 had risen in rank over several older males, M79 had risen in rank over one older male, and two adult males (M32 and M61) had risen in rank over another adult male (M29). Despite these changes, M99 was the recipient of only two agonistic acts by other males during the first 23 weeks of the 1978 breeding season (1978A), and was significantly higher-ranking than the male with the next highest cardinal rank, M15 (xZ=3.73, df=l, P < 0.055). During the 24th and 25th weeks of the 1978 breeding season (1978B), M99 and M15 were challenged and defeated in a series of intense polyadic agonistic encounters with a number of the males they had previously dominated. M61, M32 and M29 were also able to defeat M99 and M 15 in dyadic agonistie encounters, and thereby became higher-ranking than M99 and M15. In the remainder of the 1978 breeding season these three males initiated 81.3% of the 187 agonistic acts we observed among males. The majority of their aggressive acts were directed toward M99 and M 15 (78/152---51.3 %). In contrast, these three males rarely acted aggressively toward one another (2/152= 1.3 %), and M99 and M15 never directed aggression toward each other (0/26). Although M29 remained the topranking male until the beginning of the next breeding season, a period of 30 weeks, his cardinal dominance rank was not significantly different from the cardinal ranks of the two males who ranked below him, M61 and M32 (X2=0.88, df=2, P > 0.50). M61 replaced M29 as the top-ranking male at the beginning of the 1979 breeding season, and maintained that position until the end of our

998

ANIMAL

BEHAVIOUR,

study, a period of 11 months. M61's cardinal dominance rank was not significantly different from that of M29, who ranked immediately below him (X2=2.13, df= 1, P<0.154). The stability of the male dominance hierarchy during our study is reflected by (1) the length of time each of the top-ranking males maintained their positions, (2) the magnitude of the difference in cardinal rank between adjacent highranking males, and (3) the number and frequency of changes in the rank order. M99 was the topranking male for more than 5 years, M29 for 30 weeks, and M61 for at least 11 months. M99 was the only one of these three top-ranking males whose cardinal dominance rank was significantly different from that of the male who ranked immediately below him. No changes in the rank order occurred during the 1977 breeding season, but in each of the two subsequent breeding seasons several males changed ranks. Thus, by all three measures, the dominance hierarchy was more stable in 1977 than in 1978 or 1979.

B. Associations between Males and Conceiving Females In 1977, three of the six focal females (F34, F47 and F38) associated exclusively during their conception periods with a single male significantly more often than with all other males combined. M99, the top-ranking male, was the primary companion of each of these females (Fig. 2). None of the other three focal females associated during their conception periods exclusively with a single male significantly more than with all other males. M32 was the most common companion of two of these females, F12 and F44; M48, a subadult male who died later in the same breeding season, was the most common companion of F19. Six focal females had conceived before M99 was challenged and defeated in 1978. M99 was the primary companion of one of these females (F47) during her conception period, and M61 was the primary companion of the other (F34). The other four conceiving females did not associate during their conception periods with their most common companions significantly more often than with all other males. After M99 was challenged and defeated in 1978, two focal females conceived. M29 and M61 were the primary companions of F21 and F38, respectively, during their conception periods. During the 1979 breeding season, none of the five focal females who conceived were accompanied during their conception periods by a

32,

4

single male significantly more often than by all other males. While two of these females (F34 and F47) had primary companions in previous years, the other three females ( F l l , F41 and F44) did not.

C. Responsiblity for Proximity between Males and Conceiving Females Exclusive associations between males and conc'eiving females might be expected to occur simply because males rarely associate with one another, as is the case in many cercopithecine species (M. fuscata: Grewal 1980; M. mulatta: Lindburg 1971; Papio ursimts: Saayman 1971; Seyfarth 1978). Male bonnet macaques, however, associate with each other often (Simonds 1963, 1965). On 28.6% of all 30-s intervals during the 1978 and 1979 breeding seasons (9748/34 080 intervals), at least one male was within 3 m of the focal male. Moreover, at least one female was present on 72.6% of those intervals in which males were in proximity to one another (7079/ t978A

1977 54 47581244 19

'~176 !ml

1978B

54 47 II 4441 19

1979

o 21 58

~ 54 47 II 44 41

O~

d

o~

3z~l-q-~

99__ 99~

I00

8 o~ z9 ioo

"~oI~176 I -Ld '~

0

22

"0

24

~oo~

o~ ' ' ~ 1 7 6E

,oOo 48__ ~ 2 o

zg~r'q_4~

~

22 ~]

24

~

1 5 ~

79

~

22 ~ _

29 ~

~

24 _ _

~5

['-']

r-l--,

24 ~

Fig. 2. Exclusive proximity to females during conception periods. Each bar corresponds to the percentage of all intervals of exclusive proximity to a given female for which each male was responsible. Column totals are equal to 100%. In each time period, males and females are listed in decreasing rank order. Primary companionships, denoted by dark bars, were identified by the procedure described in the text (normal approximation of the binomial test, P< 0.003 in all cases). Point-sample data from 1977 are not presented in this figure. These data are in agreement with focal-sample data for F34, F47 and F38 (in all cases, P<0.001) and for F12 (P=0.324), but are not in agreement with focal-sample data for F44 (focal sample, P=0.003; point sample, P=0.749) or for FI9 (focal sample, P=0.001; point sample, P=0.271). Because of the very small sample of focal observations (particularly of F19) in 1977, primary companionships were identified only when both data sets were in agreement.

SAMUELS ET AL.: CHANGES IN RANK AND MATING 9748 intervals). Thus the formation of exclusive associations between males and conceiving females is not an artifact of the spatial distribution of males. To evaluate the role of males and conceiving females in maintaining proximity to one another, we have calculated values of the Hinde-Atkinson index (Hinde & Atkinson 1970). This index represents the difference between the proportion of 'approaches' and 'leaves' initiated by each individual in a particular dyad. The absolute value of the index indicates the extent of each partner's contribution, and the sign of the index indicates which partner is primarily responsible for maintaining proximity. Here, negative indices indicate that the male is primarily responsible for maintaining proximity. Primary companions played a larger role in maintaining proximity to their conceiving female companions than did the most common companions of conceiving females. Primary companions collectively initiated 94.0% and terminated only 34.1% of all bouts of proximity with their conceiving female companions (HindeAtkinson index=--0.58). Although the most common companions of conceiving females initiated fewer (71.6%) and terminated slightly more (38.7%) bouts of proximity than did primary companions, the value of the HindeAtkinson index (--0.36) indicates that these males were still principally responsible for maintaining proximity to females. Taken together, these results suggest that exclusive associations between males and conceiving females generally occurred as males followed females. D. Benefits to Males of Forming Exclusive Associations with Conceiving Females

Only males who maintained exclusive proximity to conceiving females had the opportunity to copulate, as copulations rarely occurred when two males were near each other. In only 8.3 % of 277 copulations was a second male within 3 m of the copulating pair. Thus, primary companions, who were in exclusive proximity to conceiving females significantly more often than other males, had significantly more time in which to copulate with their conceiving female partners than did other males. In contrast, the most common companions of other conceiving females did not have significantly more time to copulate with their female companions than did other males. There is some evidence that primary companions did copulate with their conceiving

999

female companions more often than did other males. Conceiving females copulated with their primary companions significantly more often than expected by chance alone (binomial test; 1977:N=2 copulations, P=0.028; 1978 : N= 12, P=0.001). In contrast, conceiving females did not copulate with their most common companions any more often than expected (1977: N = 0 ; 1978: N=3, P=0.37; 1979: N=7, P = 0.219). Conceiving females copulated with their primary companions relatively more often (10/14 copulations= 71.4 %) than other conceiving females copulated with their most common companions (3/10=30~; Fisher exact test: P = 0.048). Thus, primary companions were the males who were most likely to associate and copulate with their conceiving female companions. E. Selectivity in Male Mate Choice

Males primarily maintained exclusive proximity to and copulated with high-ranking females. All seven of the females who had primary companions were high-ranking (range= ranks 1-12). The five high-ranking females in our sample conceived a total of 11 times during the course of the study period. During seven of these conception periods, females had primary companions. In contrast, four low-ranking females in our sample conceived a total of eight times (one low-ranking female did not conceive). None of these females had primary companions during their conception periods (Fisher exact test: P = 0.007). In 1978 and 1979, males copulated with cycling and conceiving high-ranking females significantly more often than with cycling and conceiving low-ranking females (201/258 total copulations = 77.9 %). F. The Relationship between Male Rank and Access to Females

All the primary companions were high-ranking males (range=ranks 1-3). High-ranking males spent more time in exclusive proximity to highranking females than did low-ranking males. In 1977, 1978A and 1978B, male rank was positively correlated with the cumulative proportion of exclusive proximity to conceiving high-ranking females (Spearman rank correlation coefficients: 1977: rs=0.77, P=0.051; 1978A: rs=0.68, P = 0.055; 1978B: rs=0.89, P=0.006; 1979; rs= 0.38, P=0.18; Fig. 3). High- and low-ranking males generally spent similar amounts of time in proximity to conceiving low-ranking females. Male dominance rank was unrelated to the

1000

ANIMAL

~ 100[-"

1977

I/

E~ ~ ~ -

I

BEHAVIOUR,

1978A

I

rs = 0.77

32,

4

1978B

1979

rs = 0.89*

l\

"~

9

/.\ o

-

"---

1254567

It

~-, i , i

1 2 54

h ,

5 13-~ 1 2 3 4 Maledominancerank

56f

[I

i

12345678

i"r/,,

Fig. 3. The relationship between male rank and exclusive proximity to conceiving high-ranking females. In each graph, the vertical axis represents the percentage of exclusive proximity to all conceiving high-ranking females for which males of each dominance rank were responsible. *P< 0.055. cumulative proportion of exclusive proximity to conceiving low-ranking females in 1977, 1978A and 1978B (1977: r s = --0.257, P = 0 . 1 6 3 ; 1978A: rs=0.036, P = 0 . 4 8 2 ; 1978B: no low-ranking females conceived; 1979: rs = --0.667, P=0.048). Prior to conception and during the period of probable conception, females copulated primarily with the first-, second- and third-ranking males (187/258 copulations=72.5%). Male dominance rank was positively related to the proportion of all copulations with cycling and conceiving females in 1977 (rs = 0.783, P = 0.046), 1978A (rs=0.636, P=0.069), 1978B (rs=0.955, P=0.003) and 1979 (rs=0.786, P=0.014). G. Changes in the Rank and Mating Behaviour of Males The frequency with which individual males gained exclusive access to conceiving females changed during the study period as the rank ordering of males changed. The males who rose furthest in rank experienced the greatest increases in exclusive proximity to conceiving high-ranking females, and the males who fell furthest in rank experienced the greatest reductions in exclusive proximity to conceiving high-ranking females (Table II; 1977 to 1978: rs =0.926, P = 0.01 ; 1978 to 1979; rs=0.631, P=0.073). Males who rose in rank were also responsible for progressively greater proportions of copulations, while males who dropped in rank were responsible for fewer copulations. For example, M99 was responsible for 46 % of all copulations with cycling a n d conceiving females in 1977,

when he was the top-ranking male; 31% in 1978, when he fell from first to fourth-ranking male; and only 7 9/00in 1979, as he remained the fourthranked male. In contrast, M61, the third-ranked male in 1977 and the top-ranked male in 1979, was responsible for 15 9/00of all copulations with cycling and conceiving females in 1977, 19 % in 1978 and 29 % in 1979. This pattern is even more pronounced when only copulations with highranking cycling and conceiving females are conTable H. Changesin Rank and Association with Conceiving High-ranking Females

1977 to 1978 Changes in:

M99 M29 M61 M32 M22 M24 M15

Rank*

Access (%)1"

--3 --3+4=-t-1 +1 +1 --2 --2 +2

--71.4 +23.7 +30.5 + 11.2 0.0 -- 0.1 no data

1978 to 1979 Changes in: Access Rank++ (%)w 0 --1 +1 0 +1 0 --2

--12.8 --15.8 + 1.3 + 2.4 +12.0 + 5.4 -- 2.2

*1978B rank minus 1977 rank. tProportion of exclusive proximity to conceiving highranking females in 1978B minus proportion of exclusive proximity to conceiving high-ranking females in 1977. Data for 1978A and 1978B were combined and averaged. No focal observations were conducted on M15 in 1977. ++1979 rank minus 1978B rank. w of exclusive proximity to conceiving highranking females in 1979 minus proportion of exclusive proximity to conceiving females in 1978B. Data for 1978A and 1978B were combined and averaged.

SAMUELS ET AL.: CHANGES IN RANK AND MATING sidered (Fig. 4). It is particularly notable that M99 never copulated with cycling or conceiving high-ranking females after he was challenged and defeated in 1978. Discussion The dominance rank of adult males consistently influenced their patterns of association and sexual interactions with cycling and conceiving females. Only high-ranking males became the primary compamons of conceiving females. These males, who spent significantly more time in exclusive proximity to their conceiving female partners than did all other males combined, were significantly more likely to copulate with their female partners than were any other males. The three highest-ranking males were responsible for nearly three-quarters of all copulations with cycling and conceiving females. High-ranking males formed exclusive associations and copulated primarily with females who were highranking. In contrast, low-ranking males were more opportunistic and less successful in their mating efforts. They associated and copulated primarily with low-ranking females, but they did not become primary companions, and rarely copulated with conceiving females. Changes in dominance rank were directly related to changes in the mating behaviour of males. Males who rose in rank spent increasing amounts of time in exclusive proximity to conceiving high-ranking females, and copulated with cycling and conceiving females more often than before. For males whose ranks declined, the pattern was reversed. The relationship between male rank and mating behaviour varied over the course of the study period. In 1977, the top-ranking male was rarely confronted by lower-ranking males, and no males changed ranks. In that year, the topranking male was able to monopolize access to 1977

d

d

1978

6 ~ 2 9 ~

29 61

d 99 29 61

52

52

52

22 24

22 24 L5

22 24 15 79

99

]

1979

I j

0 rO 20 30 40 0 10 20 30 40 20 40 50 Percentage of Copulotions with Cycling and Conceiving High-Ranking Femoles

Fig. 4. Percentageof copulationswith all cyclingand conceiving high-ranking females. Each bar represents the percentageof all copulationswiththosefemalesfor which a single male was responsible. Males are listed in 1977 (descending) rank order.

1001

conceiving high-ranking focal females, and male dominance rank was correlated with exclusive proximity to conceiving high-ranking females and copulations with cycling and conceiving females. During the 1978 breeding season, several rank changes preceded the challenge and defeat of the top-ranking male. Although dominance rank was correlated with exclusive proximity to conceiving high-ranking females and copulations with all cycling and conceiving females during the 1978 breeding season, no single male was able to monopolize access to conceiving females. During the 1979 breeding season no males became primary companions of conceiving females, and male dominance rank was unrelated to exclusive access to conceiving high-ranking females. Thus, 1977 was an unusual year for two reasons: (1)the dominance hierarchy was more stable than in other years, and (2) the top-ranking male monopolized access to high-ranking females more effectively than did any of the males who subsequently held that position. High-ranking males associated and mated selectively with high-ranking females. Assortative mating by rank may enhance the fitness of high-ranking males. This is because the offspring of high-ranking females are more likely to survive than are the offspring of low-ranking females in this group of bonnet macaques (Silk et al. 1981a), and in captive and semi-freeranging groups of rhesus macaques, M. mulatta (Drickamer 1974; Sade et al. 1976; Wilson et al. 1978). This means that high-ranking males associated and copulated with the females who were most likely to produce surviving offspring. Given that male mating behaviour varied over the course of our study, it is perhaps not surprising that our findings are at variance with some published accounts of the behaviour of bonnet macaques. In particular, it has been reported that free-ranging bonnet macaque males rarely form consortships, and that highranking males do not have preferential access to receptive females (Simonds 1963, 1965; Rahaman & Parthasarathy 1969; Sugiyama 1971). However, these patterns were not quantified and females were assumed to be receptive whenever copulations were observed. Simonds (1963) also noted that the top-ranking male was deposed during the breeding season, indicating that male rank relations may have been unstable during some part of his study. Shively et al. (1982) investigated mating behaviour of males in the CPRC bonnet macaque group during the year

1002

ANIMAL

BEHAVIOUR,

after our study ended, and reported that male rank was negatively correlated with the proportion of copulations for which each male was responsible. Their analysis did not take into account the reproductive state of the females with whom males copulated, and their conclusions were based upon a small sample of copulations. Moreover, it is unlikely that male rank relations were stable during their 3-month study, because four adult males (including the two highest-ranked males in 1980) were removed from the group at the beginning of their study period. Although it is not possible to determine whether these discrepancies represent actual differences in mating behaviour or artifacts of the differences in observational methods and analytic techniques, some of the patterns we describe are consistent with those found in other studies of cercopithecine primates. Glick (1980) observed the same group of bonnet macaques during the first year of our study, and found that high-ranking males were most likely to form consortships and to copulate with high-ranking females during the month in which the females conceived. High-ranking Japanese macaque males (M. fuscata) form extended associations with a few females, while low-ranking males associate briefly with many females (Fedigan & Gouzoules 1978). Recent studies of captive macaques, in which the paternity of infants is determined from serological markers, indicate that in stable social groups male rank is positively correlated with the number of live-born infants sired (Duvall et al. 1976; Smith 1980, 1981; Witt et al. 1981). Studies of baboons that focus upon mating behaviour at the time females are most likely to conceive also indicate that high-ranking males mate with conceiving females more often than do low-ranking males (P. cynocephalus: Hausfater 1975; P. ursinus: Seyfarth 1978; P. anubis: Packer 1979): Japanese macaques are also reported to mate assortatively by rank (Stephenson 1975; Fedigan & Gouzoules 1978), although rhesus macaques apparently do not (Small & Smith 1982). The data presented here suggest that several dimensions of male dominance relationships influenced the relationship between male rank and reproductive performance. In particular, the stability of male rank relations appeared to influence the nature of this relationship, such that high-ranking males obtained the greatest reproductive advantage when the dominance hierarchy was most stable.

32,

4

Although the correlation between male dominance rank and reproductive success is well substantiated, we know very little about the factors that influence that relationship. Before general conclusions about the relationship between male dominance rank and reproductive success can be drawn, more must be known about the behavioural strategies by which males achieve reproductive success, the form and nature of dominance relationships among males, and the social and ecological factors that influence dominance .relationships. Both methodological and empirical issues must be resolved before this can be accomplished. For example, quantitative measures of dominance that can be compared over time and across species are needed (Boyd & Silk 1983), as is cross-sectional and longitudinal information about male reproductive performance and fitness (cf. Hausfater 1975). Acknowledgments This research was conducted at the California Primate Research Center, University of California, Davis, and was supported in part by USPHS Grant RR00169. JBS was supported by a Regents fellowship from the University of California and an NSF postdoctoral fellowship during the period of data collection and analysis. We would like to thank Dr Barbara B. Glick for generously providing unpublished data. We also thank a number of colleagues for comments upon the manuscript: S. A. Altmann, J. Altmann, L. Berenstain, W. J. Hamilton, A. Hedrick, W. A. Mason and K. S. Smith. REFERENCES Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour, 44, 227-267. Bielert, C., Czaja, J. A., Eisele,S., Schemer,G., Robinson, J. A. & (Joy, R. W. 1976. Mating in the rhesus monkey (Macaca mulatta) after conception and its relationship to oestradiol and progesterone levels throughout pregnancy. Y. Reprod. Fert., 46, 179-187. Boyd, R. & Silk, J. B. 1983. A method for assigning cardinal dominance ranks. Anita. Behav., 31, 45-58. Dewsbury, D. 1982. Dominance rank, copulatory behavior, and differentialreproduction. Q. Rev. Biol., 57, 135-159. Driekamer, L. C. 1974. A ten-year summary of reproductive data for free ranging Macaca mulatta. Folia Prirnat., 21, 61-80. Duvall, S. W., Bernstein, I. S. & Gordon, T. P. 1976. Paternity and status in a rhesus monkey group. J. Reprod. Fert., 47, 25-31. Fedigan, L. & Gouzoules, H. 1978. The consort relationship in a troop of Japanese monkeys. In: Recent Advances in Primatology, VoL 1 : Behaviour (Ed. by D. J. Chivers & J. Herbert), pp. 493--496. New York: Academic Press.

SAMUELS ET AL.: CHANGES IN R A N K A N D MATING Glick, B. B. 1980. Ontogenetic and psychobiological aspects of the mating activities of male Macaca radiata. In: The Macaques: Studies in Ecology, Behavior and Evolution (Ed. by D. G. Lindburg), pp. 345-369. New York: Van Nostrand Reinhold. Grewal, B. S. 1980. Social relationships between adult central males and kinship groups of Japanese monkeys at Arashiyama, with some aspects of troop organization. Primates, 21, 161-180. I-Iausfater, G. 1975. Dominance and reproduction in baboons (Papio cynocephalus): a quantitative analysis. Contrib. Primat., 7. Basel: S. Karger. Hendrickx, A. G. & Binkerd, P. E. 1979. Primate teratology: selection of species and future use. In: Advances in the Study of Birth Defects, Vol. 2 (Ed. by T. V. N. Persaud), pp. 1-23. Lancaster, England: MTP Press. Hinde, R. A. & Atkinson, S. 1970. Assessing the roles of social partners in maintaining mutual proximity, as exemplified by mother-infant relations in rhesus monkeys. Anita. Behav., 18, 169-176. Judge, D. S. & Rodman, P. S. 1976. Macaca radiata: intragroup relations and reproductive status of females. Primates, 17, 535-539. Lindburg, D. G. 1971. The rhesus monkey in N. India: an ecological and behavioral study. In: Primate Behavior: Developments in Field and Laboratory Research, Vol. 2 (Ed. by L. A. Rosenblum), pp. 2-106. New York: Academic Press. MacDonald, G. J. 1971. Reproductive patterns of three species of macaques. Fert. Steril., 22, 373-377. Nigi, H. 1976. Some aspects related to conception of the Japanese monkey. Primates, 17, 81-87. Packer, C. 1979. Male dominance and reproductive activity in Papio anubis. Anita. Behav., 27, 37-45. Parkin, R. F. & Hendrickx, A. G. 1975. The temporal relationship between the preovulatory estrogen peak and the optimal mating period in rhesus and bonnet monkeys. Biol. Reprod., 13, 610-616. Rahaman, H. & Parthasarathy, M. D. 1969. Studies of the social behavior of bonnet monkeys. Primates, 10, 149-162. Saayman, G. S. 1971. Behavior of the adult males in a troop of free-ranging chacma baboons (Papio ursinus). Folia primat., 15, 36-57. Sade, D. S., Cushing, K., Cushing, C., Dunaif, J., Figueroa, A., Kaplan, J. R., Lauer, C., Rhodes, D. & Schneider, J. 1976. Population dynamics in relation to social structure on Cayo Santiago. Yrbk phys. Anthropol., 20, 253-262. Seyfarth, R. M. 1978. Social relationships among adult male and female baboons: I. Behaviour during sexual consortship. Behaviour, 64, 204-226. Shively, C., Clarke, S., King, N., Schapiro, S. & Mitchell, G. 1982. Patterns of sexual behavior in male macaques. Am. Y. PrimatoL, 2, 373-384.

1003

Silk, J. B. 1982. Altruism among female Maeaea radiata: explanations and analysis of patterns of grooming and coalition formation. Behaviour, 79, 162-188. Silk, J. B., Clark-Wheatley, C., Rodman, P. S. & Samuels, A. 1981a. Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata). Anim. Behav., 29, 1106-1120. Silk, J. B., Samuels, A. & Rodman, P. S. 1981b. Hierarchical organization of female Macaca radiata. Primates, 22, 84-95. Simonds, P. E. 1963. Ecology of macaques. Ph.D. thesis, University of California at Berkeley. Simonds, P. E. 1965. The bonnet macaque in South India. In: Primate Behavior (Ed. by I. DeVote), pp. 175-196. New York: Holt, Rinehart & Winston. Simpson, J. S. 1976. Social integration of male Macaca radiata. Ph.D. thesis, University of California at Davis. Small, M. F. & Smith, D. G. 1982. The relationship between maternal and paternal rank in rhesus macaques (Macaca mulatta). Anim. Behav., 30, 626-627. Smith, D. G. 1980. Paternity exclusion in six captive groups of rhesus monkeys (Macaca mulatta). Am. J. phys. Anthropol., 53, 243-249. Smith, D. G. 1981. The association between rank and reproductive success of male rhesus monkeys. Am. J. PrimatoL, 1, 83-90. Stabenfeldt, G. H. & Hendrickx, A. G. 1972. Progesterone levels in the bonnet monkey (Maeaca radiata) during the menstrual cycle and pregnancy. Endocrinology, 91, 614-619. Stephenson, G. R. 1975. Social structure of mating activity in Japanese macaques. In: Contemporary Primatology: Proceedings from the Fifth Congress of the International Primatological Society (Ed. by S. Kondo, M. Kawai, A. Ehara & J. Kawamura), pp. 63-116. Tokyo: Japan Science Press. Sugiyama, Y. 1971. Characteristics of the social life of bonnet macaques (Maeaea radiata). Primates, 12, 247-266. Wilson, M. E., Gordon, T. P. & Bernstein, I. S. 1978. Timing of births and reproductive success in rhesus monkey social groups. J. med. Primatol., 7, 202-212. Witt, R., Schmidt, C. & Schmitt, J. 1981. Social rank and Darwinian fitness in a multimale group of Barbary macaques (Maeaea sylvana): dominance reversals and male reproductive success. Folia primat., 36, 201-211.

(Received 4 November 1982; revised 2 December 1983; MS. number: A3065)