- Email: [email protected]
Male dominance and reproductive activity in Papio anubis
Anion.
Behav.,
MALE
1979, 21, 37-45
DOMINANCE
AND REPRODUCTIVE
ACTIVITY
IN PAPlO ANUBIS
BY C. PACKER Department of Biology, University of Sussex, Brighton, Sussex BN1 9QG
Abstract. The dominance relations of the sexually mature males residing in three troops of Papio am&is at Gombe National Park, Tanzania are examined and three tactics which males employed to increase temporarily their dominance against other males are discussed. The summation of the dominance relationships in each troop revealed a linear hierarchy. In immigrant (‘transferred’) males, dominance rank was highly correlated with reproductive activity and the alpha male in each troop was likely to have fathered a disproportionately large number of offspring. However, the alpha males did not father all offspring conceived during the study, and factors other than dominance which affected male reprod;ctiv< activity are also-considered. Although much has been written about the relationship between male dominance and male reproductive success in primates, few studies have been of sufficient detail or duration, or have concerned a large enough sample of individuals to provide strong evidence for or against this relationship. Difficulties also arise in studies where overall reproductive activity is measured, and the short period of maximal fertility in the female is not or cannot be considered. High ranking males may mate most frequently during the period of maximal fertility (Ransom 1971; Hausfater 1975) and low ranking males may mate more frequently than high ranking males with females outside this period (Stephenson 1974; Packer 1978). Where dominance is the only factor governing male access to females, the dominant (‘alpha’) male would always be able to gain access to any female at maximal fertility in his troop, and only when there is more than one such female available at a time would a subordinate male be able to gain access to one (Altmann 1962). Whenever the relationship between dominance and reproductive activity is not perfect, an examination of other variables affecting male reproductive success is necessary, but an extensive consideration of such variables has not yet been made. The detailed study reported here concerned a larger population and extended over a longer period than had been considered in previous studies of Pupio spp. The correlation between dominance and reproductive activity in fullsized males was high but not perfect, and a series of variables is considered which may have increased the reproductive success of subordinate males relative to that of alpha males.
are given in Packer 1977a and 1978. Data concern 27 sexually mature males in three different troops in Gombe National Park, Tanzania. Sexually mature males who were known or assumed to have transferred into their troop of residence are referred to as ‘transferred males’; sexually mature males residing in their natal troop are ‘natal males’. Twenty-five of these males were observed regularly on a ‘focal sample’ basis (Altmann 1974) either between May and December 1972 or between June 1974 and May 1975. Data on the reproductive activity of all males were taken from the ‘attendance data’ which were collected on most days during the study periods and included a record of the reproductive state of each female and the identity of the consort partners for each oestrous female. These data are available from May 1972 to May 1976 and some information on dominance relations dates from November 1967. Assessment of Dominance Relationships The assessment of dominance relationships was based on supplants of one male by another, primarily because of their high frequency. Visibility at Gombe was so low in most parts of the troops’ ranges that regular ad libitum sampling could not be made reliably, and malemale threats were so uncommon that focal sample observations of threats were inadequate by themselves to provide interaction matrices in all the troops under study. Tn each interaction between two males, one animal was designated as ‘active’ and the other as ‘passive’, depending on which male first moved directly towards the other. During the interaction, the passive male was observed to see if he moved away from the active male; either by jumping back a few inches or walking away from him. If the passive male moved away from the active male, he was recorded as
Methods Background information on the study population and descriptions of the sampling procedures 37
ANIMAL
38
BEHAVIOUK,
having ‘yielded’, if he did not move away, he was recorded as having ‘maintained’. The dominance relationship between a pair of males (male A and male B) was determined by taking the number of times A ‘yielded’ (AY), A ‘maintained’ (AM), B ‘yielded’ (BY) and B ‘maintained’ (BM) and calculating: (1) The relative success rate in supplanting AY
BY BM+BY
(2) The corrected
proportion
of ‘yields’
AY = 2(-.--- 0.5) 4Y+ BY
The second measure is corrected so that its range of values equals the range of the first measure (+ 1 .O to - 1.O). For both measures the sign of the resultant value indicates which individual in the pair is dominant: if positive, B is dominant to A, if negative, A is dominant to B. In 84.1% of male-male pairs (n = 151>, the same male was found to be dominant by both measures. Therefore, the male that had the higher success rate in supplanting the other also supplanted him more often than vice versa. Pairs in which the two measures did not agree were either those for whom very few interactions were observed or those where the data probably included false decisions (i.e. a male happened to walk away while being advanced upon, but not as a direct result of that advance). For these pairs the measure with the highest absolute value in each pair was used by convention to designate which individual in that pair was the dominant one. After the dominance relationship had been determined within each pair, the assessments were compared with displacements from feeding sites-defined as when one male took over a food source from another male. In 93.8% of male-male pairs (n = 96) the male that had taken over a feeding site from the other more often was also the male that had been labelled dominant on the basis of the maintain-yield criterion. Therefore, dominance as measured here reflected an ability to gain access to feeding sites in competition with other males. Dominance assessments do not include interactions between males when: (1) The active male screamed at the passive male.
27.
I
(2) Either male was carrying an infant. (3) Either male was consorting with an oestrous female. These three factors consistently reversed the outcome of interactions between two males: (1) In 11 of 14 pairs of males the active male was more likely to supplant the passive male when he screamed at him than when he did not scream at him. Sometimes a screaming male would chase away a male that was ordinarily dominant to him. (2) In 17 of 20 pairs of males, a male increased his relative dominance (either by being more able to supplant the other or being himself less likely to be supplanted) against the other by carrying an infant. (3) When male A was consorting with an oestrous female and B was not, A was dominant to B; but when B was consorting and A was not. B was dominant to A (T = 1, n = 7 independent matched pairs of males, P < 0.05, Wilcoxon; i.e. 14 males each appear only once in the test). Occasionally males would form sudden consortships with females when they were being threatened by other males and this had the effect of terminating the aggression of the other males. The advantage gained from using these tactics lasted only for as long as the male continued to scream, carry an infant, or consort; and once the two males came back into contact after a prior interaction with a ‘reversal factor’ their basic dominance relationship remained unchanged. Also, these tactics were not infallible. They usually had the effect of inhibiting aggression in the opponent, but screaming males and males carrying infants were sometimes attacked, and consorting males were sometimes fought in contests over access to the oestrous female. (A male carrying an infant was less likely to receive a threat during an interaction with another male than when he was not carrying an infant (20 of 22 pairs).) Determination of Overall Dominance Rank The basic dominance relationships for all sexually mature males in each troop (including those that were not focal sample subjects) are shown in Table I. In each incomplete matrix the rows and columns are ordered with the minimum number of reversals in an assumed linear ‘hierarchy’. A computer simulation designed by Dr P. H. Harvey was used to test each ordered matrix for linearity. The simulation considered an n x n matrix specifying the number and location of cells for which there were
PACKER:
MALE
DOMINANCE
AND
REPRODUCTIVE
no data. It then randomly assigned one member of each pair as dominant and the other as subordinate. After 100 to 300 runs, it was determined whether the observed data produced
BRM
BRM YLL* COL ORE* MON B Troop 1972: GRN EBN CRS MRY* BBB* DVD BRM* JNH YMZ* MSS
YLL* .,
COL
ORE+ ~I
IN PAP10
ANUBfS
39
an ordered matrix with fewer reversals than an ordered random matrix formulated by the computer. For three of the four matrices, the observed data were significantly linear (i.e.
Table I. Dominance Matrix A Troop:
ACTIVITY
from Each Troop
MON in
t GRN
EBN
CRS
MRY*
BBB*
DVD 1,~
a: -.
-
B Troop 19744975: EBN EBN JNH GRN LEO CRS KKT MDK DVD MSS HML
-~ -.
JNH
YMZ*
~, I
-:
\
LEO
CRS
KKT
MDK
DVD
-, 7
\
-1. ,:
MSS
HML
_..
GRN
MSS
1 -1 \I~
I
JNH
BRM*
QSQ*
STP
ASG *
-II-
i.
.-
..-:
1s:
w
+
r
ASG* C Troop:
WTH
BBB
YMZ
MNT
WDY
GNG
LEO
HML*
MDK
css
FRD*
WTH BBB YMZ MNT WDY GNG LEO HML* MDK css FRD+ Rankings in A troop and B troop 1972 are based on number of males each row male dominated: rankings in B troop 19741975 and C troop are based on order which was most ‘linear’ (see text). i denotes row animal is dominant to column animal. ~~ denotes row is subordinate to column. * denotes natal male.
40
ANIMAL
REHAVIOUR,
contained fewer reversals than 2.5% of the random runs (P < 0.05, two-tailed)). The dominance matrix for A troop was perfectly linear, but contained too few individuals to provide a statistically significant result. Dominance ranks are based on the number of males dominated by each male in the two complete dominance matrices (B troop 1972 and A troop), but are based on the ordered matrices in the two incomplete dominance matrices (B troop 1974 to 1975 and C troop), because of the high degree of linearity found. Dominance ranks reflect the average dominance of each individual over each study period. Although the dominance ranking of each established transferred male appeared to be relatively stable, there may have been many changes amongst subordinate males which could not have been detected from the small amount of data that could be collected over a short period in each troop (for consideration of recent immigrants and of natal males. see Packer 1978). However, ‘alpha’ males almost certainly maintained their rank for long periods. Each male indicated to have been alpha in each troop in Table I was also considered subjectively to have been alpha by other observers, and to have been alpha both at the beginning and the end of each study period. The alpha male in B troop in 1972, GRN, was believed to have become alpha in 1968 (Ransom 1971) and apparently continued to be alpha until April 1974, and several other alpha males remained alpha for up to three years (L. T. Nash, A. Sindimwo, J. I. Oliver, personal communication). Dominance and Reproductive Activity
Male Papio an&s form exclusive consortships with oestrous females in which they copulate frequently with the female and prevent her from interacting with other males. Consortships were formed on the third day prior to detumescence (D-3), the day on which copulations are most likely to result in conception (Hendrickx & Kraemer 1969) in virtually every fertile cycle. One male could sometimes monopolize a female for her entire period of maximum tumescence, including night-time (Packer 1978). The reproductive activity of each transferred male was measured by finding the proportion of days each male consorted with oestrous females during the study periods out of the total number of days all of the oestrous females in his troop were consorted by any male. ‘Natal males’ are excluded from this analysis because of
27,
1
their extremely low reproductive activity, which appeared to result from avoiding inbreeding (Packer 1978). All sexually mature transferred males were full-sized adults. Consorting activity was significantly correlated with dominance rank in transferred males (i; = 0.80, z = 2.98, P < 0.003, Kraemer test, Kraemer 1975, based on Spearman correlations from each troop). During the study periods 21 pregnancies occurred and the consorting activity of transferred males on D-3 of these ‘fertile cycles’ was also significantly correlated with dominance rank ($ = 0.58, z -:m:2.17, P < 0.03). Hausfater (1975) reported a similar correlation for D--3 in all cycles of Papio cynocephalus. In 15 of 21 cases in this study the alpha male in the troop consorted with the female on D-3 in fertile cycles (Table XI in Packer 1978). Hausfater found that the alpha male in his study troop did not consort on D-3 in any of three such cycles, and Cheney & Seyfarth (1977) reported that the alpha male in a troop of Pupio ursinus with only two adult males consorted on D-3 in six of eight such cycles. Alpha males at Gombe also consorted more on D-3 and D-2 than on other days in the females’ fertile cycles (Table XII in Packer 1978). Other Variables Affecting Activity
Male
Reproductive
Although dominance was an important factor in determining a male’s reproductive success, it was unlikely to have been the only factor. In four of the six fertile cycles in which the female was not consorted by the alpha male on D-3. she was the only female consorted in that troop on that day and she was consorted by males known never to have been alpha. Observations of aggressive encounters between males over oestrous females suggested several variables which may have reduced the consorting success of the alpha male in each troop. These include : 1. Asymmetry of contest. The effect of consorting on the dominance relationship between two males was described earlier. A consorting male was avoided by other males regardless of their usual dominance relationships. Kummer et al. (1974) reported a similar response to pairs of Papio hamadryas. This probably reflects the consorting male’s willingness to fight in order to maintain access to his female. Hausfater (1975) reported that most serious wounds inflicted on adult male Papio cvnocephalus occurred when an oestrous female was present in the troop:
PACKER:
MALE
DOMINANCE
AND
REPRODUCTIVE
similarly in Macaca mulatta and Macaca sinica most serious wounds on males are inflicted during the mating season (Wilson & Boelkins 1970; Dittus 1977). In Macaca jiuscata intense aggression between males appears to be rare and being in consort does not provide an advantage in maintaining the female (Stephenson 1974). In an encounter between two Papio anubis males, being in consort may provide an asymmetry wherein the consorting male often ‘wins’ encounters without having to fight (Maynard Smith & Parker 1976). A ‘biased asymmetry’ would result if the female had a higher value to the consorting male than to the rival (e.g. if II males had copulated with the female during her period of peak fertility, the nth male would have a l/n chance of siring the resultant offspring, the (n -t 1)th male would have a l/(n + 1) chance, and since ljrt > l/(n + l), the holder would always have higher prospects of paternity than the rival), or if the consorting male had a greater probability of keeping the female after the encounter than the rival had of taking her over (e.g. female Theropithecus gelada sometimes refuse to accept a new male who has defeated or replaced their harem leader, Mori & Kawai 1974; U. Mori, personal communication). Thus, possession of an oestrous female may often exceed the importance of dominance rank (except when the discrepancy between males is very large). In 78 of 110 cycles, subordinate males started consorting earlier in the female’s cycle than did more dominant males (P < 0.01, sign test). This resulted in dominant males having to overcome the asymmetry in order to gain access to the female. 2. Mobility. Physical size may be an important attribute in competition for stationary resources such as food, but there are probably limits in size above which manoeuvrability is reduced, and the latter may be important in competition for a mobile oestrous female. Dominance rank was correlated with body weight in full-sized males (Packer 1978), but consorting activity was not. There was one high ranking male who was so large and slow-moving that other males could easily outmaneouvre him in contests over oestrous females, and, perhaps as a result, his rank in consorting activity was much lower than his dominance rank. Consort changeovers commonly occurred in two general situations which required high mobility in the participants. First, changeovers at Gombe frequently resulted from encounters of coalitions of two or more males with the
ACTIVITY
IN PAP10
ANUBIS
51
consorting male. In these, one or more of the coalition members continued to fight the consorting male while his partner ran to the female (Packer 1977b). Some consorting males were able to withstand the efforts of coalitions, either by moving the female away from the vicinity of the coalition, or by manipulating the coalition partners into threatening someone else. Second, young males were able to take over oestrous females from older competitors by outmanoeuvring them in sleeping trees (D. A. Collins & L. T. Nash, personal communication ; personal observation). These males leapt from branch to branch in attempts to separate the consorting male from his female. 3. Coalitions. When the formation of a coalition resulted in the take-over of an oestrous female from a consorting male, it was the male who initiated the coalition who received the female (in all six cases) and not necessarily the dominant male of the pair (the dominant male gained the female in three out of six cases). Coalition formation is reciprocated (Packei 1977b), so the correlation between dominance and consorting activity is necessarily reduced. 4. Experience. Of the seven males of above average age for transferred males whose dominance rank was not the same as their intra-troop rank in consorting activity, six ranked higher in consorting activity than in dominance (T = I. n = 7, P < 0.05). One possible explanation is that experience increases consorting ability. Competition for oestrous females often involved complex manipulations of conspecifics as well as the recognition and avoidance of potentially hazardous situations which could result in changeovers. Thus, the males with the most experience in consorting may have been able to manage such situations the best, and older males who were once alpha would be expected to compete for females more successfully than would be predicted from their current dominance rank. 5. Wounds. Fights between males over accessto oestrous females were common, but only rarely resulted in wounding. However, males occasionally received severe wounds which adversely affected their subsequent competitive ability. Between 1967 and 1976 one male died from wounds received in a fight (since May 1976 another male is believed to have died from a fight over an oestrous female, J. Goodall, personal communlcation) and two males lost the sight of one eye. Between 1972 and 1975 five males received deep gashes. At least three males limped for several
4’
ANIMAL
BEHAVIOUK,
months after receiving injury, and others were debilitated for shorter periods. Such damage appeared to decrease their consort success more than their dominance rank. Three injured highranking males continued to be avoided by subordinates but showed reduced consorting activity until their wounds were nearly healed. 6. Canine condition. Competition for oestrous females could not only increase the probability of receiving a severe wound, but could also decrease the ability to inflict such a wound. Canine teeth began to emerge at about 66 to 72 months of age and deep wounds could only be inflicted by males whose canines were virtually intact. Canines wear down (canine condition in males with fully erupted canines versus age: I’s L - 0.85. n = 20, P < O.OOl), though they were not used in feeding or catching mammalian prey (personal observation) and only rarely in defence against chimpanzees (Wrangham 1975). The main cause of canine wear at Gombe was probably breakage in fights. Males occasionally interlocked canines during intense fights and this was once seen to result in the chipping off of a large section of one of the antagonist’s canines. Two males with very poor canines for their age were the alpha males in their respective troops and they may have worn down their canines in gaining and maintaining their high rank. Males displayed their canines by exaggerated, non-directed yawning and Darwin (1890, page 145) reported that a captive baboon no longer yawned after having his canines sawn off. The frequency with which transferred males displayed their canines by non-directed yawning when within 5 m of other transferred males was significantly correlated with the condition of the drsplaying male’s canines (rs = 0.54, n p= 14. P < O-05), but not significantly correlated with his age. The frequency of canine displays which occurred when no other male was within 5 m was not significantly correlated with the condition of the displaying male’s canines. Thus, males with the best canines displayed them most often to other males, and males, therefore, had the opportunity to apppraise each other’s canines. The success of young males in taking away oestrous females in sleeping trees seemed also to be related to the consorting male’s feal of the younger male’s sharp canines. There were three pairs of males of approximately the same age that were comprised of individuals with canines of very different quality. In each of these three pans. the male wrth the bettel
37,
I
canines was also the male with the higher overall consorting activity. 7. Fatigue. Consorting can intlict costs on the consorting male beyond the direct costs of competition (Hausfater 1975). Feeding patterns are different in males and females in Pupio anubis (Oliver, in preparation) and the transferred males in the current study spent significantly less time feeding while consorting than 12, II I=- 15. when they were not consorting (T P -I 0.01). Males spent a median of 17.5”/;, of the time feeding during consortships and 27.4 s,, outside consortships. In red deer (Cervus rlaphus), stags cease feeding during the rut and body weight decreases rapidly (Mitchell et al. 1976). Baboon consortships persisted through the night; copulations were frequent (12 times in 12 hours during one night-long observation period. J. l. Oliver, personal communication) and the male continued to show possessive behaviour (J. Morris, personal communication). It is therefore likely that a male slept and fed less than usual while consorting, and became exhausted from maintaining continual proximity with his consort and vigilance in avoiding potential rivals. There are probably physical limits beyond which a male cannot continue to consort. One of the functions of harassment of a consort pair by a rival may therefore be to tire out the consorting male. ‘Harassment’ refers to maintaining close proximity to the consorting pair and/or threatening the pair from a distance during copulations. Whereas a rival male may rest or feed after persistently harassing the consorting male, the latter must continue keeping up with the female.
8. Male selectivity and female choice. Consorting may be rare between certain combinations of males and females as a result of (1) males selecting particular females with whom to consort, as in iMucacafuscuta (Stephenson 1974) and in Pupio cynocephuhs (Hausfater 1975) (2) females preferring a particular male to be consorted by, thus influencing his success in maintaining her, as in Pan trog/o&te.~ (Tutin 1976). By selecting particular females, a male may increase his probability of fathering their offspring. either by increasing the co-operation of those females during consortships (see below) or by a greater willingness to fight in order to maintain access to them. By persistently selecting a particular female, a male may have a ‘consorting asymmetry more clearly biased in his favour.
PACKER:
MALE
DOMINANCE
AND
REPRODUCTIVE
and thus be more successful in encounters with rivals. The preference of the female for a particular male may not be correlated with his dominance rank (Saayman 1971; Bernstein 1976), but may reflect the female’s relationship with the male when they are not consorting (e.g. Saayman 1971; Seyfarth 1975; Tutin 1976). In this study, four of twelve males who resided in a single troop long enough to be tested showed significant selectivity in consorting with particular females between 1972 and 1976 [Table II). Three of these four males were in one troop, and they tended to select different females from each other (Fig. I). The selectivity of these four males was related to their social relationships with the females outside consortships. Selectivity for particular females was significantly correlated with the frequency that the four males groomed each female per minute within 5 m of her outside consortships in 1974 to 1975 (i; = 0.37, z = 2.58, P < 0.01). Consorting selectivity was also significantly correlated with percentage of time spent within 5 m of the female outside consortships (6 = 0.37, z = 2.7 17 P < O-01). The latter result was at least partly due to the behaviour of the females since consorting selectivity of the male was significantly correlated with the extent to which the female
ACTIVITY
IN PAP10
ANUEIS
maintained proximity to him (measured by finding the difference in percentages between approaches and leaves at S m from the male, Hinde & Atkinson 1970) (ii = 0.29, z L= 2.03, P < 0.05). Those females with whom a male consorted most were those who were most active in maintaining proximity to him. This is not the result of females showing preference for one male over others: a positive correlation was found in only eight of fourteen females in B troop, between the extent to which each female maintained proximity to each of the three males in her troop with significant consorting selectivitiy and the extent to which each male selected that female to consort with. Consorting selectivity by these males was not significantly correlated with either the female’s dominance rank or her age; neither for all four males combined nor for any one of them. This suggests that the consorting selectivity of each male may depend more on the selectivity of other males than on factors associated with the female. The behaviour of the female was not general]) an obvious factor in determining which transferred male consorted with her; although she could sometimes determine which males did not continue to consort with her, either by frequently approaching other males or by avoiding her
Table II. Consorting Selectivity of Males EBN
AP: AR: AZ: BT: CF: CL: HM: JA: LO: MG: MR:
Yes
No
Yes
10 11
0 I;:
5 11
3
WA :
No
JNH Yes
1;:
AW: FU: GA: g.: JU; LU: MI: PA: PS: TA: TH:
1
3
7
;
4 10
3: 17
2; 11
i
:
%
6
30 3 0
:i 7
2 5
2 3
4 Pi 9 3 3
.:
2
x 2 12 4
: 10 4
G = 85.19,
G = 24.65
13 de!L
12df P c : 0.07
P -.: 00Il
GNG -Yes No
No
9
Fz
2;; SS:
GRN
4:;
G -- 16.01
2 rlf
P -; 0.01
G = 8.95. 3 d/l I’ -c 0.05
Numbers under each male are the number of consorted cycles that the male consorted with the row female (Yes) and the number of cycles that the male did not consort with her (No) during the time that that male was present in the troop. Bold numbers are for those families that cycled sufficiently to be used in a k ,: r G Test.
ANIMAL
44
BEHAVIOUR,
Females : AP AR AZ BT CF CL HM JA LO MG MR QU RO SS WA 0 1 E c, Xl’ ,? _ ‘23 Males : x := EBN ~2 -_ GRN O-JNH Fig. 1. The four females consorted for the highest proportion of cycles by each of the three males showing significant consorting selectivity in B troop (see Table II). The females BT, CF, and QU were the oldest in the troop.
while he was being threatened by other males (see also Packer 1978). Males appeared to cultivate co-operative relationships with females, and they tended to consort most with those females with whom they had the most co-operative relationships (see above). The investment males made in cultivating females appeared to increase with age: transferred males groomed with females more frequently as they became older (Packer 1977a). This may have been because fighting ability decreases with age. In Pan troglodytes, low-ranking males are able to form consortships with females that they have groomed frequently, while highranking males are able to monopolize females without actively cultivating their co-operation (Tutin 1976). partner
Summary
The observed correlation between dominance rank and consorting activity in transferred males was high and the ‘alpha’ male in each troop probably sired a disproportionately large number of offspring. However, there are several factors which may decrease the consorting success of the dominant male to less than lOO,y<. Many of these relate to the monopolization of a mobile resource over several days and the tactics as well as consequences of aggressive competition.
Acknowledgments
Field work was supported by grants from the Ford Foundation and the W.T. Grant Foundation. I am grateful to the authorities of the Tanzania National Parks for permission to work in Gombe National Park and Dr Jane Goodall fur providing facilities in the Gombe Stream Research Centre and access to data collected after the termination of my field study. I am also
37,
I
grateful to all those individuals responsible for the continuity of the long-term records on the baboons. I thank Dr Tim Clutton-Brock, Anthony Collins, Dr Paul Harvey, Dr Jeff Kurland, Professor John Maynard Smith. Dr Anne Pusey, and Dr Robert Seyfarth for advice, help and discussion. Finally 1 thank Joan Pusey for careful proof-reading. REFERENCES
Altmann, J. 1974. Observational study of behaviour. Sampling methods. Behaviour, 49, 227-267. Altmann, S. A. 1962. A field study of the sociobiology of the rhesus monkey, Macacn mulatto. Ann. N. Y. Acad.
Sci.,
102,
338-435.
Bernstein, I. S. 1976. Dominance, aggression and reproduction in primate societies. J. theor. Biol.. 60. 459-472.
Cheney, D. L. & Seyfarth, R. M. 1977. Behaviour of adult and immature male baboons during intergroup encounters. Nature, Lo&., 269, 404-406. Darwin, C. R. 1890. The Expression of the Emotions i/l Man and Animds, 2nd edn. London: Murray. Dittus, W. P. J. 1977. The social regulation of population density and age-sex distribution in the toque monkey. Behaviour, 63, 281-322. Hausfater, G. 1975. Dominance and reproduction in baboons (Papio cynocephalus): a quantitative analysis. Contrib. Primatol., 7. Basel: Karger. Hendrickx, A. G. & Kraemer, D. C. 1969. Observations on the menstrual cycle, optimal mating time and pre-implantation embryos of the baboon, Papio cmubis and Papio cynocephniu.c. J. Reprod. Fertil. Suppl., 6, 119-128. Hinde. R. A. & Atkinson, S. 1970. Assessing the role\ of social partners in maintaining mutual proximity, as exemplified by mother/infant relations in monkeys. Anim. Behav., 18, 169-176. Kracmer, H. C. 1975. On estimation and hypothesis testing problems for correlation coefficients. Psychometrika,
40, 473-485.
Kummer, H., Gotz, W. & Angst, W. 1974. Triadic differentiation: an inhibitory process protecting pair bonds in baboons. Behaviour, 49, 62-87. Maynard Smith, J. & Parker, G. A. 1976. The logic of asymmetric contests. Anim. Behczv.. 24, 159-175. Mitchell, B., McGowan, D. & Nicholson, I. A. 1976. Annual cycles of body weight and condition in Scottish red deer, Cerws elnphus. J. Zoo/., 180, 107-127. Mori, U. Sr.Kawai, M. 1974. Social relations and behavior of Gelada baboons. Crlnten?p. Primot., 5th Int.
Conw.
Primat..
470-474.
Oliver. J. I. (in Greparation). Behavioural ecology in baboons in Tanzania. Ph.D. Thesis. Cambridge University. Packer, C‘. 1977a. Inter-troop transfer and inbrecdlnf avoidance in PnDio ur7ubi.r in Tanzania. Ph.1) Thesis. Universit) of Sus>e\. Packer, C. 1977b. Reciprocal ;tltrui\m 111/‘opb) o/lril~i\. Nature,
Land.,
265,
44 I-443.
Packer, (‘. 1978. Inter-troop transfer .md mblecdmy iivoidance in Papio anubis. Anim. Behnv., 27, l-30. Ransom. T. W. 1971. Ecology and social behavior of baboons in Gombe Stream National Park. Ph.D. ‘Thesis, University of California. Berkeley.
PACKER:
MALE
DOMINANCE
AND
REPRODUCTIVE
Saayman. G. S. 1971. Behaviour of the adult males in a troop of free-ranging chacma baboons (Pupio ursinus). Folia. Primatol.. 15, 36-57. Scyfarth. R. M. 1975. The social relationships among adults in a troop of free-ranging baboons (Pupio cvnocephahrs c/rslnra). Ph.D. Thesis, Cambridge University. Stephenson,, G. R. 1974. Social structure of mating activitv in Jauanese macaaues. ,‘hno. 5f/z cona. Int’l ikmat. koc. (Ed. by 3. Kondd, M. Kaws. A. Ehara & S. Kawamura), pp. 63-l 15. Tokyo: Japan Science Press.
ACTIVlTY
IN PAPIO
ANC’R1.S
Tutin.
45
C. E. G. 1976. Sexual behaviour and mating pattern5 in a communit,y of wild chimpanzees fPan troglodytes schweir,firrthii). Ph.D. Thesis, University of Edinburgh. W~lhon, A. I’. 6i Boelkins, R. c’. 1970. Evidence for seasonal variation in aggressive behaviour b:.l Macaca mlrlatta. Anim. Behav., 18, 719-724. Wrangham, R. W. 1975. The behavioural ecology 01 chimpanzees in Gombe National Park, Tanzania. Ph.D. Thesis, Cambridge University. (Received 2 August 1977; revised 1 1Iforcl1 1978; MS. number: 1725)
Behav.,
MALE
1979, 21, 37-45
DOMINANCE
AND REPRODUCTIVE
ACTIVITY
IN PAPlO ANUBIS
BY C. PACKER Department of Biology, University of Sussex, Brighton, Sussex BN1 9QG
Abstract. The dominance relations of the sexually mature males residing in three troops of Papio am&is at Gombe National Park, Tanzania are examined and three tactics which males employed to increase temporarily their dominance against other males are discussed. The summation of the dominance relationships in each troop revealed a linear hierarchy. In immigrant (‘transferred’) males, dominance rank was highly correlated with reproductive activity and the alpha male in each troop was likely to have fathered a disproportionately large number of offspring. However, the alpha males did not father all offspring conceived during the study, and factors other than dominance which affected male reprod;ctiv< activity are also-considered. Although much has been written about the relationship between male dominance and male reproductive success in primates, few studies have been of sufficient detail or duration, or have concerned a large enough sample of individuals to provide strong evidence for or against this relationship. Difficulties also arise in studies where overall reproductive activity is measured, and the short period of maximal fertility in the female is not or cannot be considered. High ranking males may mate most frequently during the period of maximal fertility (Ransom 1971; Hausfater 1975) and low ranking males may mate more frequently than high ranking males with females outside this period (Stephenson 1974; Packer 1978). Where dominance is the only factor governing male access to females, the dominant (‘alpha’) male would always be able to gain access to any female at maximal fertility in his troop, and only when there is more than one such female available at a time would a subordinate male be able to gain access to one (Altmann 1962). Whenever the relationship between dominance and reproductive activity is not perfect, an examination of other variables affecting male reproductive success is necessary, but an extensive consideration of such variables has not yet been made. The detailed study reported here concerned a larger population and extended over a longer period than had been considered in previous studies of Pupio spp. The correlation between dominance and reproductive activity in fullsized males was high but not perfect, and a series of variables is considered which may have increased the reproductive success of subordinate males relative to that of alpha males.
are given in Packer 1977a and 1978. Data concern 27 sexually mature males in three different troops in Gombe National Park, Tanzania. Sexually mature males who were known or assumed to have transferred into their troop of residence are referred to as ‘transferred males’; sexually mature males residing in their natal troop are ‘natal males’. Twenty-five of these males were observed regularly on a ‘focal sample’ basis (Altmann 1974) either between May and December 1972 or between June 1974 and May 1975. Data on the reproductive activity of all males were taken from the ‘attendance data’ which were collected on most days during the study periods and included a record of the reproductive state of each female and the identity of the consort partners for each oestrous female. These data are available from May 1972 to May 1976 and some information on dominance relations dates from November 1967. Assessment of Dominance Relationships The assessment of dominance relationships was based on supplants of one male by another, primarily because of their high frequency. Visibility at Gombe was so low in most parts of the troops’ ranges that regular ad libitum sampling could not be made reliably, and malemale threats were so uncommon that focal sample observations of threats were inadequate by themselves to provide interaction matrices in all the troops under study. Tn each interaction between two males, one animal was designated as ‘active’ and the other as ‘passive’, depending on which male first moved directly towards the other. During the interaction, the passive male was observed to see if he moved away from the active male; either by jumping back a few inches or walking away from him. If the passive male moved away from the active male, he was recorded as
Methods Background information on the study population and descriptions of the sampling procedures 37
ANIMAL
38
BEHAVIOUK,
having ‘yielded’, if he did not move away, he was recorded as having ‘maintained’. The dominance relationship between a pair of males (male A and male B) was determined by taking the number of times A ‘yielded’ (AY), A ‘maintained’ (AM), B ‘yielded’ (BY) and B ‘maintained’ (BM) and calculating: (1) The relative success rate in supplanting AY
BY BM+BY
(2) The corrected
proportion
of ‘yields’
AY = 2(-.--- 0.5) 4Y+ BY
The second measure is corrected so that its range of values equals the range of the first measure (+ 1 .O to - 1.O). For both measures the sign of the resultant value indicates which individual in the pair is dominant: if positive, B is dominant to A, if negative, A is dominant to B. In 84.1% of male-male pairs (n = 151>, the same male was found to be dominant by both measures. Therefore, the male that had the higher success rate in supplanting the other also supplanted him more often than vice versa. Pairs in which the two measures did not agree were either those for whom very few interactions were observed or those where the data probably included false decisions (i.e. a male happened to walk away while being advanced upon, but not as a direct result of that advance). For these pairs the measure with the highest absolute value in each pair was used by convention to designate which individual in that pair was the dominant one. After the dominance relationship had been determined within each pair, the assessments were compared with displacements from feeding sites-defined as when one male took over a food source from another male. In 93.8% of male-male pairs (n = 96) the male that had taken over a feeding site from the other more often was also the male that had been labelled dominant on the basis of the maintain-yield criterion. Therefore, dominance as measured here reflected an ability to gain access to feeding sites in competition with other males. Dominance assessments do not include interactions between males when: (1) The active male screamed at the passive male.
27.
I
(2) Either male was carrying an infant. (3) Either male was consorting with an oestrous female. These three factors consistently reversed the outcome of interactions between two males: (1) In 11 of 14 pairs of males the active male was more likely to supplant the passive male when he screamed at him than when he did not scream at him. Sometimes a screaming male would chase away a male that was ordinarily dominant to him. (2) In 17 of 20 pairs of males, a male increased his relative dominance (either by being more able to supplant the other or being himself less likely to be supplanted) against the other by carrying an infant. (3) When male A was consorting with an oestrous female and B was not, A was dominant to B; but when B was consorting and A was not. B was dominant to A (T = 1, n = 7 independent matched pairs of males, P < 0.05, Wilcoxon; i.e. 14 males each appear only once in the test). Occasionally males would form sudden consortships with females when they were being threatened by other males and this had the effect of terminating the aggression of the other males. The advantage gained from using these tactics lasted only for as long as the male continued to scream, carry an infant, or consort; and once the two males came back into contact after a prior interaction with a ‘reversal factor’ their basic dominance relationship remained unchanged. Also, these tactics were not infallible. They usually had the effect of inhibiting aggression in the opponent, but screaming males and males carrying infants were sometimes attacked, and consorting males were sometimes fought in contests over access to the oestrous female. (A male carrying an infant was less likely to receive a threat during an interaction with another male than when he was not carrying an infant (20 of 22 pairs).) Determination of Overall Dominance Rank The basic dominance relationships for all sexually mature males in each troop (including those that were not focal sample subjects) are shown in Table I. In each incomplete matrix the rows and columns are ordered with the minimum number of reversals in an assumed linear ‘hierarchy’. A computer simulation designed by Dr P. H. Harvey was used to test each ordered matrix for linearity. The simulation considered an n x n matrix specifying the number and location of cells for which there were
PACKER:
MALE
DOMINANCE
AND
REPRODUCTIVE
no data. It then randomly assigned one member of each pair as dominant and the other as subordinate. After 100 to 300 runs, it was determined whether the observed data produced
BRM
BRM YLL* COL ORE* MON B Troop 1972: GRN EBN CRS MRY* BBB* DVD BRM* JNH YMZ* MSS
YLL* .,
COL
ORE+ ~I
IN PAP10
ANUBfS
39
an ordered matrix with fewer reversals than an ordered random matrix formulated by the computer. For three of the four matrices, the observed data were significantly linear (i.e.
Table I. Dominance Matrix A Troop:
ACTIVITY
from Each Troop
MON in
t GRN
EBN
CRS
MRY*
BBB*
DVD 1,~
a: -.
-
B Troop 19744975: EBN EBN JNH GRN LEO CRS KKT MDK DVD MSS HML
-~ -.
JNH
YMZ*
~, I
-:
\
LEO
CRS
KKT
MDK
DVD
-, 7
\
-1. ,:
MSS
HML
_..
GRN
MSS
1 -1 \I~
I
JNH
BRM*
QSQ*
STP
ASG *
-II-
i.
.-
..-:
1s:
w
+
r
ASG* C Troop:
WTH
BBB
YMZ
MNT
WDY
GNG
LEO
HML*
MDK
css
FRD*
WTH BBB YMZ MNT WDY GNG LEO HML* MDK css FRD+ Rankings in A troop and B troop 1972 are based on number of males each row male dominated: rankings in B troop 19741975 and C troop are based on order which was most ‘linear’ (see text). i denotes row animal is dominant to column animal. ~~ denotes row is subordinate to column. * denotes natal male.
40
ANIMAL
REHAVIOUR,
contained fewer reversals than 2.5% of the random runs (P < 0.05, two-tailed)). The dominance matrix for A troop was perfectly linear, but contained too few individuals to provide a statistically significant result. Dominance ranks are based on the number of males dominated by each male in the two complete dominance matrices (B troop 1972 and A troop), but are based on the ordered matrices in the two incomplete dominance matrices (B troop 1974 to 1975 and C troop), because of the high degree of linearity found. Dominance ranks reflect the average dominance of each individual over each study period. Although the dominance ranking of each established transferred male appeared to be relatively stable, there may have been many changes amongst subordinate males which could not have been detected from the small amount of data that could be collected over a short period in each troop (for consideration of recent immigrants and of natal males. see Packer 1978). However, ‘alpha’ males almost certainly maintained their rank for long periods. Each male indicated to have been alpha in each troop in Table I was also considered subjectively to have been alpha by other observers, and to have been alpha both at the beginning and the end of each study period. The alpha male in B troop in 1972, GRN, was believed to have become alpha in 1968 (Ransom 1971) and apparently continued to be alpha until April 1974, and several other alpha males remained alpha for up to three years (L. T. Nash, A. Sindimwo, J. I. Oliver, personal communication). Dominance and Reproductive Activity
Male Papio an&s form exclusive consortships with oestrous females in which they copulate frequently with the female and prevent her from interacting with other males. Consortships were formed on the third day prior to detumescence (D-3), the day on which copulations are most likely to result in conception (Hendrickx & Kraemer 1969) in virtually every fertile cycle. One male could sometimes monopolize a female for her entire period of maximum tumescence, including night-time (Packer 1978). The reproductive activity of each transferred male was measured by finding the proportion of days each male consorted with oestrous females during the study periods out of the total number of days all of the oestrous females in his troop were consorted by any male. ‘Natal males’ are excluded from this analysis because of
27,
1
their extremely low reproductive activity, which appeared to result from avoiding inbreeding (Packer 1978). All sexually mature transferred males were full-sized adults. Consorting activity was significantly correlated with dominance rank in transferred males (i; = 0.80, z = 2.98, P < 0.003, Kraemer test, Kraemer 1975, based on Spearman correlations from each troop). During the study periods 21 pregnancies occurred and the consorting activity of transferred males on D-3 of these ‘fertile cycles’ was also significantly correlated with dominance rank ($ = 0.58, z -:m:2.17, P < 0.03). Hausfater (1975) reported a similar correlation for D--3 in all cycles of Papio cynocephalus. In 15 of 21 cases in this study the alpha male in the troop consorted with the female on D-3 in fertile cycles (Table XI in Packer 1978). Hausfater found that the alpha male in his study troop did not consort on D-3 in any of three such cycles, and Cheney & Seyfarth (1977) reported that the alpha male in a troop of Pupio ursinus with only two adult males consorted on D-3 in six of eight such cycles. Alpha males at Gombe also consorted more on D-3 and D-2 than on other days in the females’ fertile cycles (Table XII in Packer 1978). Other Variables Affecting Activity
Male
Reproductive
Although dominance was an important factor in determining a male’s reproductive success, it was unlikely to have been the only factor. In four of the six fertile cycles in which the female was not consorted by the alpha male on D-3. she was the only female consorted in that troop on that day and she was consorted by males known never to have been alpha. Observations of aggressive encounters between males over oestrous females suggested several variables which may have reduced the consorting success of the alpha male in each troop. These include : 1. Asymmetry of contest. The effect of consorting on the dominance relationship between two males was described earlier. A consorting male was avoided by other males regardless of their usual dominance relationships. Kummer et al. (1974) reported a similar response to pairs of Papio hamadryas. This probably reflects the consorting male’s willingness to fight in order to maintain access to his female. Hausfater (1975) reported that most serious wounds inflicted on adult male Papio cvnocephalus occurred when an oestrous female was present in the troop:
PACKER:
MALE
DOMINANCE
AND
REPRODUCTIVE
similarly in Macaca mulatta and Macaca sinica most serious wounds on males are inflicted during the mating season (Wilson & Boelkins 1970; Dittus 1977). In Macaca jiuscata intense aggression between males appears to be rare and being in consort does not provide an advantage in maintaining the female (Stephenson 1974). In an encounter between two Papio anubis males, being in consort may provide an asymmetry wherein the consorting male often ‘wins’ encounters without having to fight (Maynard Smith & Parker 1976). A ‘biased asymmetry’ would result if the female had a higher value to the consorting male than to the rival (e.g. if II males had copulated with the female during her period of peak fertility, the nth male would have a l/n chance of siring the resultant offspring, the (n -t 1)th male would have a l/(n + 1) chance, and since ljrt > l/(n + l), the holder would always have higher prospects of paternity than the rival), or if the consorting male had a greater probability of keeping the female after the encounter than the rival had of taking her over (e.g. female Theropithecus gelada sometimes refuse to accept a new male who has defeated or replaced their harem leader, Mori & Kawai 1974; U. Mori, personal communication). Thus, possession of an oestrous female may often exceed the importance of dominance rank (except when the discrepancy between males is very large). In 78 of 110 cycles, subordinate males started consorting earlier in the female’s cycle than did more dominant males (P < 0.01, sign test). This resulted in dominant males having to overcome the asymmetry in order to gain access to the female. 2. Mobility. Physical size may be an important attribute in competition for stationary resources such as food, but there are probably limits in size above which manoeuvrability is reduced, and the latter may be important in competition for a mobile oestrous female. Dominance rank was correlated with body weight in full-sized males (Packer 1978), but consorting activity was not. There was one high ranking male who was so large and slow-moving that other males could easily outmaneouvre him in contests over oestrous females, and, perhaps as a result, his rank in consorting activity was much lower than his dominance rank. Consort changeovers commonly occurred in two general situations which required high mobility in the participants. First, changeovers at Gombe frequently resulted from encounters of coalitions of two or more males with the
ACTIVITY
IN PAP10
ANUBIS
51
consorting male. In these, one or more of the coalition members continued to fight the consorting male while his partner ran to the female (Packer 1977b). Some consorting males were able to withstand the efforts of coalitions, either by moving the female away from the vicinity of the coalition, or by manipulating the coalition partners into threatening someone else. Second, young males were able to take over oestrous females from older competitors by outmanoeuvring them in sleeping trees (D. A. Collins & L. T. Nash, personal communication ; personal observation). These males leapt from branch to branch in attempts to separate the consorting male from his female. 3. Coalitions. When the formation of a coalition resulted in the take-over of an oestrous female from a consorting male, it was the male who initiated the coalition who received the female (in all six cases) and not necessarily the dominant male of the pair (the dominant male gained the female in three out of six cases). Coalition formation is reciprocated (Packei 1977b), so the correlation between dominance and consorting activity is necessarily reduced. 4. Experience. Of the seven males of above average age for transferred males whose dominance rank was not the same as their intra-troop rank in consorting activity, six ranked higher in consorting activity than in dominance (T = I. n = 7, P < 0.05). One possible explanation is that experience increases consorting ability. Competition for oestrous females often involved complex manipulations of conspecifics as well as the recognition and avoidance of potentially hazardous situations which could result in changeovers. Thus, the males with the most experience in consorting may have been able to manage such situations the best, and older males who were once alpha would be expected to compete for females more successfully than would be predicted from their current dominance rank. 5. Wounds. Fights between males over accessto oestrous females were common, but only rarely resulted in wounding. However, males occasionally received severe wounds which adversely affected their subsequent competitive ability. Between 1967 and 1976 one male died from wounds received in a fight (since May 1976 another male is believed to have died from a fight over an oestrous female, J. Goodall, personal communlcation) and two males lost the sight of one eye. Between 1972 and 1975 five males received deep gashes. At least three males limped for several
4’
ANIMAL
BEHAVIOUK,
months after receiving injury, and others were debilitated for shorter periods. Such damage appeared to decrease their consort success more than their dominance rank. Three injured highranking males continued to be avoided by subordinates but showed reduced consorting activity until their wounds were nearly healed. 6. Canine condition. Competition for oestrous females could not only increase the probability of receiving a severe wound, but could also decrease the ability to inflict such a wound. Canine teeth began to emerge at about 66 to 72 months of age and deep wounds could only be inflicted by males whose canines were virtually intact. Canines wear down (canine condition in males with fully erupted canines versus age: I’s L - 0.85. n = 20, P < O.OOl), though they were not used in feeding or catching mammalian prey (personal observation) and only rarely in defence against chimpanzees (Wrangham 1975). The main cause of canine wear at Gombe was probably breakage in fights. Males occasionally interlocked canines during intense fights and this was once seen to result in the chipping off of a large section of one of the antagonist’s canines. Two males with very poor canines for their age were the alpha males in their respective troops and they may have worn down their canines in gaining and maintaining their high rank. Males displayed their canines by exaggerated, non-directed yawning and Darwin (1890, page 145) reported that a captive baboon no longer yawned after having his canines sawn off. The frequency with which transferred males displayed their canines by non-directed yawning when within 5 m of other transferred males was significantly correlated with the condition of the drsplaying male’s canines (rs = 0.54, n p= 14. P < O-05), but not significantly correlated with his age. The frequency of canine displays which occurred when no other male was within 5 m was not significantly correlated with the condition of the displaying male’s canines. Thus, males with the best canines displayed them most often to other males, and males, therefore, had the opportunity to apppraise each other’s canines. The success of young males in taking away oestrous females in sleeping trees seemed also to be related to the consorting male’s feal of the younger male’s sharp canines. There were three pairs of males of approximately the same age that were comprised of individuals with canines of very different quality. In each of these three pans. the male wrth the bettel
37,
I
canines was also the male with the higher overall consorting activity. 7. Fatigue. Consorting can intlict costs on the consorting male beyond the direct costs of competition (Hausfater 1975). Feeding patterns are different in males and females in Pupio anubis (Oliver, in preparation) and the transferred males in the current study spent significantly less time feeding while consorting than 12, II I=- 15. when they were not consorting (T P -I 0.01). Males spent a median of 17.5”/;, of the time feeding during consortships and 27.4 s,, outside consortships. In red deer (Cervus rlaphus), stags cease feeding during the rut and body weight decreases rapidly (Mitchell et al. 1976). Baboon consortships persisted through the night; copulations were frequent (12 times in 12 hours during one night-long observation period. J. l. Oliver, personal communication) and the male continued to show possessive behaviour (J. Morris, personal communication). It is therefore likely that a male slept and fed less than usual while consorting, and became exhausted from maintaining continual proximity with his consort and vigilance in avoiding potential rivals. There are probably physical limits beyond which a male cannot continue to consort. One of the functions of harassment of a consort pair by a rival may therefore be to tire out the consorting male. ‘Harassment’ refers to maintaining close proximity to the consorting pair and/or threatening the pair from a distance during copulations. Whereas a rival male may rest or feed after persistently harassing the consorting male, the latter must continue keeping up with the female.
8. Male selectivity and female choice. Consorting may be rare between certain combinations of males and females as a result of (1) males selecting particular females with whom to consort, as in iMucacafuscuta (Stephenson 1974) and in Pupio cynocephuhs (Hausfater 1975) (2) females preferring a particular male to be consorted by, thus influencing his success in maintaining her, as in Pan trog/o&te.~ (Tutin 1976). By selecting particular females, a male may increase his probability of fathering their offspring. either by increasing the co-operation of those females during consortships (see below) or by a greater willingness to fight in order to maintain access to them. By persistently selecting a particular female, a male may have a ‘consorting asymmetry more clearly biased in his favour.
PACKER:
MALE
DOMINANCE
AND
REPRODUCTIVE
and thus be more successful in encounters with rivals. The preference of the female for a particular male may not be correlated with his dominance rank (Saayman 1971; Bernstein 1976), but may reflect the female’s relationship with the male when they are not consorting (e.g. Saayman 1971; Seyfarth 1975; Tutin 1976). In this study, four of twelve males who resided in a single troop long enough to be tested showed significant selectivity in consorting with particular females between 1972 and 1976 [Table II). Three of these four males were in one troop, and they tended to select different females from each other (Fig. I). The selectivity of these four males was related to their social relationships with the females outside consortships. Selectivity for particular females was significantly correlated with the frequency that the four males groomed each female per minute within 5 m of her outside consortships in 1974 to 1975 (i; = 0.37, z = 2.58, P < 0.01). Consorting selectivity was also significantly correlated with percentage of time spent within 5 m of the female outside consortships (6 = 0.37, z = 2.7 17 P < O-01). The latter result was at least partly due to the behaviour of the females since consorting selectivity of the male was significantly correlated with the extent to which the female
ACTIVITY
IN PAP10
ANUEIS
maintained proximity to him (measured by finding the difference in percentages between approaches and leaves at S m from the male, Hinde & Atkinson 1970) (ii = 0.29, z L= 2.03, P < 0.05). Those females with whom a male consorted most were those who were most active in maintaining proximity to him. This is not the result of females showing preference for one male over others: a positive correlation was found in only eight of fourteen females in B troop, between the extent to which each female maintained proximity to each of the three males in her troop with significant consorting selectivitiy and the extent to which each male selected that female to consort with. Consorting selectivity by these males was not significantly correlated with either the female’s dominance rank or her age; neither for all four males combined nor for any one of them. This suggests that the consorting selectivity of each male may depend more on the selectivity of other males than on factors associated with the female. The behaviour of the female was not general]) an obvious factor in determining which transferred male consorted with her; although she could sometimes determine which males did not continue to consort with her, either by frequently approaching other males or by avoiding her
Table II. Consorting Selectivity of Males EBN
AP: AR: AZ: BT: CF: CL: HM: JA: LO: MG: MR:
Yes
No
Yes
10 11
0 I;:
5 11
3
WA :
No
JNH Yes
1;:
AW: FU: GA: g.: JU; LU: MI: PA: PS: TA: TH:
1
3
7
;
4 10
3: 17
2; 11
i
:
%
6
30 3 0
:i 7
2 5
2 3
4 Pi 9 3 3
.:
2
x 2 12 4
: 10 4
G = 85.19,
G = 24.65
13 de!L
12df P c : 0.07
P -.: 00Il
GNG -Yes No
No
9
Fz
2;; SS:
GRN
4:;
G -- 16.01
2 rlf
P -; 0.01
G = 8.95. 3 d/l I’ -c 0.05
Numbers under each male are the number of consorted cycles that the male consorted with the row female (Yes) and the number of cycles that the male did not consort with her (No) during the time that that male was present in the troop. Bold numbers are for those families that cycled sufficiently to be used in a k ,: r G Test.
ANIMAL
44
BEHAVIOUR,
Females : AP AR AZ BT CF CL HM JA LO MG MR QU RO SS WA 0 1 E c, Xl’ ,? _ ‘23 Males : x := EBN ~2 -_ GRN O-JNH Fig. 1. The four females consorted for the highest proportion of cycles by each of the three males showing significant consorting selectivity in B troop (see Table II). The females BT, CF, and QU were the oldest in the troop.
while he was being threatened by other males (see also Packer 1978). Males appeared to cultivate co-operative relationships with females, and they tended to consort most with those females with whom they had the most co-operative relationships (see above). The investment males made in cultivating females appeared to increase with age: transferred males groomed with females more frequently as they became older (Packer 1977a). This may have been because fighting ability decreases with age. In Pan troglodytes, low-ranking males are able to form consortships with females that they have groomed frequently, while highranking males are able to monopolize females without actively cultivating their co-operation (Tutin 1976). partner
Summary
The observed correlation between dominance rank and consorting activity in transferred males was high and the ‘alpha’ male in each troop probably sired a disproportionately large number of offspring. However, there are several factors which may decrease the consorting success of the dominant male to less than lOO,y<. Many of these relate to the monopolization of a mobile resource over several days and the tactics as well as consequences of aggressive competition.
Acknowledgments
Field work was supported by grants from the Ford Foundation and the W.T. Grant Foundation. I am grateful to the authorities of the Tanzania National Parks for permission to work in Gombe National Park and Dr Jane Goodall fur providing facilities in the Gombe Stream Research Centre and access to data collected after the termination of my field study. I am also
37,
I
grateful to all those individuals responsible for the continuity of the long-term records on the baboons. I thank Dr Tim Clutton-Brock, Anthony Collins, Dr Paul Harvey, Dr Jeff Kurland, Professor John Maynard Smith. Dr Anne Pusey, and Dr Robert Seyfarth for advice, help and discussion. Finally 1 thank Joan Pusey for careful proof-reading. REFERENCES
Altmann, J. 1974. Observational study of behaviour. Sampling methods. Behaviour, 49, 227-267. Altmann, S. A. 1962. A field study of the sociobiology of the rhesus monkey, Macacn mulatto. Ann. N. Y. Acad.
Sci.,
102,
338-435.
Bernstein, I. S. 1976. Dominance, aggression and reproduction in primate societies. J. theor. Biol.. 60. 459-472.
Cheney, D. L. & Seyfarth, R. M. 1977. Behaviour of adult and immature male baboons during intergroup encounters. Nature, Lo&., 269, 404-406. Darwin, C. R. 1890. The Expression of the Emotions i/l Man and Animds, 2nd edn. London: Murray. Dittus, W. P. J. 1977. The social regulation of population density and age-sex distribution in the toque monkey. Behaviour, 63, 281-322. Hausfater, G. 1975. Dominance and reproduction in baboons (Papio cynocephalus): a quantitative analysis. Contrib. Primatol., 7. Basel: Karger. Hendrickx, A. G. & Kraemer, D. C. 1969. Observations on the menstrual cycle, optimal mating time and pre-implantation embryos of the baboon, Papio cmubis and Papio cynocephniu.c. J. Reprod. Fertil. Suppl., 6, 119-128. Hinde. R. A. & Atkinson, S. 1970. Assessing the role\ of social partners in maintaining mutual proximity, as exemplified by mother/infant relations in monkeys. Anim. Behav., 18, 169-176. Kracmer, H. C. 1975. On estimation and hypothesis testing problems for correlation coefficients. Psychometrika,
40, 473-485.
Kummer, H., Gotz, W. & Angst, W. 1974. Triadic differentiation: an inhibitory process protecting pair bonds in baboons. Behaviour, 49, 62-87. Maynard Smith, J. & Parker, G. A. 1976. The logic of asymmetric contests. Anim. Behczv.. 24, 159-175. Mitchell, B., McGowan, D. & Nicholson, I. A. 1976. Annual cycles of body weight and condition in Scottish red deer, Cerws elnphus. J. Zoo/., 180, 107-127. Mori, U. Sr.Kawai, M. 1974. Social relations and behavior of Gelada baboons. Crlnten?p. Primot., 5th Int.
Conw.
Primat..
470-474.
Oliver. J. I. (in Greparation). Behavioural ecology in baboons in Tanzania. Ph.D. Thesis. Cambridge University. Packer, C‘. 1977a. Inter-troop transfer and inbrecdlnf avoidance in PnDio ur7ubi.r in Tanzania. Ph.1) Thesis. Universit) of Sus>e\. Packer, C. 1977b. Reciprocal ;tltrui\m 111/‘opb) o/lril~i\. Nature,
Land.,
265,
44 I-443.
Packer, (‘. 1978. Inter-troop transfer .md mblecdmy iivoidance in Papio anubis. Anim. Behnv., 27, l-30. Ransom. T. W. 1971. Ecology and social behavior of baboons in Gombe Stream National Park. Ph.D. ‘Thesis, University of California. Berkeley.
PACKER:
MALE
DOMINANCE
AND
REPRODUCTIVE
Saayman. G. S. 1971. Behaviour of the adult males in a troop of free-ranging chacma baboons (Pupio ursinus). Folia. Primatol.. 15, 36-57. Scyfarth. R. M. 1975. The social relationships among adults in a troop of free-ranging baboons (Pupio cvnocephahrs c/rslnra). Ph.D. Thesis, Cambridge University. Stephenson,, G. R. 1974. Social structure of mating activitv in Jauanese macaaues. ,‘hno. 5f/z cona. Int’l ikmat. koc. (Ed. by 3. Kondd, M. Kaws. A. Ehara & S. Kawamura), pp. 63-l 15. Tokyo: Japan Science Press.
ACTIVlTY
IN PAPIO
ANC’R1.S
Tutin.
45
C. E. G. 1976. Sexual behaviour and mating pattern5 in a communit,y of wild chimpanzees fPan troglodytes schweir,firrthii). Ph.D. Thesis, University of Edinburgh. W~lhon, A. I’. 6i Boelkins, R. c’. 1970. Evidence for seasonal variation in aggressive behaviour b:.l Macaca mlrlatta. Anim. Behav., 18, 719-724. Wrangham, R. W. 1975. The behavioural ecology 01 chimpanzees in Gombe National Park, Tanzania. Ph.D. Thesis, Cambridge University. (Received 2 August 1977; revised 1 1Iforcl1 1978; MS. number: 1725)