The sociobiology of male–infant interactions in Barbary macaques,Macaca sylvanus

Anim. Behav., 1996, 51, 155–170

The sociobiology of male–infant interactions in Barbary macaques, Macaca sylvanus ANDREAS PAUL*, JUTTA KUESTER† & JOACHIM ARNEMANN‡ *Institut für Anthropologie, Universität Göttingen †Abt. Funktionelle Morphologie, Ruhr-Universität Bochum ‡Institut für Humangenetik, Klinikum der Universität Frankfurt (Received 5 December 1994; initial acceptance 25 January 1995; final acceptance 6 June 1995; MS. number: 4797)

Abstract. Unlike most Old World monkeys, male Barbary macaques frequently associate with and care for infants shortly after birth. Three functional hypotheses have been proposed to explain male–infant interactions in this and other species. (1) The ‘paternal investment hypothesis’ proposes that males invest in their own progeny or otherwise related infants, (2) the ‘mating effort hypothesis’ proposes males care for infants to increase their access to mothers, and (3) the ‘agonistic buffering hypothesis’ proposes that males use infants to regulate their relations with other males. These hypotheses were tested using data on male–infant interactions, paternity and sexual behaviour obtained during a longitudinal study on Barbary macaques living in a large outdoor enclosure. Paternity of 91 infants was determined by DNA fingerprinting. Hypothesis 1 was not supported, because males did not preferentially interact with closely related infants. Similarly, hypothesis 2 was not supported because male caretakers were not more likely to sire the next infant of the mother than non-caretakers. Hypothesis 3 was supported because (1) the direction of at least one type of triadic interactions was significantly biased towards higher-ranking males, (2) the patterning of triadic interactions was strongly dependent on the rank distance between the males, and (3) interaction frequency increased significantly during periods of high inter-male tension. While kin relations were unimportant, the use of infants familiar with the opponent suggests that males make use of their knowledge of relationships between other group members. Beyond agonistic buffering, triadic interactions may serve an important function in ? 1996 The Association for the Study of Animal Behaviour coalition formation. Owing to ample opportunity to desert their offspring, notorious paternity uncertainty and high opportunity costs, mammalian fathers are rarely expected to care for their offspring (Trivers 1972; Ridley 1978; Woodroffe & Vincent 1994). In fact, in the vast majority of species (>90%), mothers care for their young alone. Although primates are often regarded as an exception to this rule (Kleiman & Malcolm 1981), regular direct male parental care is exhibited only by a minority of species (e.g. Whitten 1987). Moreover, it is not Correspondence: A. Paul, Institut für Anthropologie, Universität Göttingen, Bürgerstraße 50, D-37073 Göttingen, Germany. J. Kuester is at the Abt. Funktionelle Morphologie, Ruhr-Universität Bochum, Postfach 102148, D-44780 Bochum, Germany. J. Arnemann is at the Institut für Humangenetik, Klinikum der Universität Frankfurt, Theodor-Stern-Kai 7, D-60596 Frankfurt/Main, Germany. 0003–3472/96/010155+16 $12.00/0

?

always clear whether ‘male care’ repesents true paternal effort or something else (Clutton-Brock 1991). Barbary macaques are especially interesting in this regard, because they appear to be the only Old World primates showing ‘intensive male caretaking’ (Whitten 1987), despite their highly promiscuous mating system (Taub 1980a; Small 1990). Three hypotheses have been proposed to explain male–infant interactions in this and other primate species. The first hypothesis assumes that male care in Barbary macaques is ‘true paternal investment’ (Taub 1980a, b, 1984, 1990), partly because almost all studies showed that males prefer to interact with certain infants, and ignore all others (Deag 1974, 1980; Taub 1984; Kuester & Paul 1986). The ‘investment hypothesis’ predicts (1) that males should associate preferentially with paternally and/or maternally related infants, 1996 The Association for the Study of Animal Behaviour

155

156

Animal Behaviour, 51, 1

and (2) that special relationships between males and infants should enhance the infants’ future survival and reproductive success. While Taub was not able to test the first prediction in his study because kin relations were unknown, he felt the second prediction was supported because the only infant in his study group with no male caretakers died of unknown causes. Kuester & Paul (1986, 1988) and Paul (1984), studying male–infant interactions in large groups of Barbary macaques with known matrilineal kin relations, rejected the investment hypothesis because males did not associate preferentially with infants of their own matriline or with putative offspring, and male ‘care’ did not improve the infants’ future survival, dominance status, or reproductive success. Further evidence against the hypothesis came from preliminary studies using DNA fingerprinting for paternity determination, which showed that paternity had no effect on the males’ preferences for specific infants (Ménard et al. 1992; Paul et al. 1992). Nevertheless, Ménard et al. (1992) speculated that paternity could be one of the variables affecting male–infant relations. The second hypothesis, developed mainly by Smuts (1985) to explain the adaptive significance of special relationships between male and female savanna baboons, suggests that ‘male care’ represents mating effort rather than paternal investment (see also Smuts & Gubernick 1992; Taub 1990, for male–infant relations in Barbary macaques). The rationale behind this hypothesis is that signalling willingness to invest in a female’s offspring would be an adaptive tactic increasing the caretaker’s chance of becoming a preferred mating partner of the infant’s mother. Whether this tactic works in Barbary macaques is not known, and genetic paternity data, necessary to test the hypothesis rigorously, have not yet been presented for any primate species. The third hypothesis was originally developed by Deag & Crook (1971), the first to observe that Barbary macaque males often carry infants towards other males. They suggested that subordinate males use infants as social tools in order to ‘stabilize or regulate their relations with those more dominant than themselves’ (Deag & Crook 1971, page 194; see also Itani 1959; Kummer 1967; Packer 1980, among others, for similar hypotheses). While Deag (1980) found evidence in support of the so-called ‘agonistic buffering hypothesis’, Taub (1980b) concluded that these interactions

were rarely a response to real or potential aggression and proposed the more neutral term ‘triadic male–infant interactions’ (see also Smith & PfefferSmith 1982). Taub (1980b, page 196) believed that ‘most triadic male–infant interactions in Barbary macaque males are a specialized ritualized subset of a comprehensive system of male–infant caretaking, so characteristic in this species’. In contrast, Kuester & Paul (1986) favoured the agonistic buffering hypothesis but presented no supporting evidence (but see Paul 1984). Although it is clear that male Barbary macaques often ‘care’ for unrelated infants (Ménard et al. 1992; Paul et al. 1992), the adaptive significance of these peculiar male–infant relations is still controversial (Taub 1990; Taub & Mehlman 1991). In this study we use behavioural and genetic evidence to test whether ‘male care’ is influenced by kinship relations, whether it increases a caretaker’s chance of siring the next infant of the mother, and whether the pattern of triadic interactions is consistent with the agonistic buffering hypothesis or other explanations. METHODS Study Site and Subjects We studied three large groups (groups B, C and F) of the Barbary macaque colony ‘Affenberg Salem’, Germany. Affenberg Salem is a 14.5-ha fenced area of mixed beech–spruce forest. The animals live outdoors throughout the year and are provisioned daily with wheat grains and fruit or vegetables spread widely on the ground at several feeding sites. The population is naturally organized into several multimale–multifemale groups whose age- and sex-composition, but not size, resemble those of wild groups (see de Turckheim & Merz 1984, for a general description; Paul & Kuester 1988, for an overview of life-history patterns and population dynamics). For management purposes, several groups were removed from the area from 1984 to 1986. Five females from these groups that could not be captured later immigrated into the study groups. Two of them were pregnant or transferred with its newborn; one followed its newborn infant that was kidnapped and adopted by a high-ranking female from another group. The use of hormonal contraceptives to reduce population growth, initiated in the mating season 1985–1986, and

Paul et al.: Male–infant interactions in macaques practised more widely from 1987 onwards, led to a strong decline in annual birth rates, from 0.81 in 1985 to 0.34 in 1988. The relevant data on group composition were as follows. Group B, observed during 1988, consisted of 82 animals, including 13 adult males (aged 7 years and older), 11 subadult males (4–6 years old) and eight infants (individuals less than 1 year old). Group F, also observed during 1988, consisted of 78 animals, including nine adult males, 11 subadult males and six infants. Group C, observed from 1985 to 1988, consisted of 92–145 animals, including 10–24 adult males, 12–22 subadult males and 14–24 infants (total: 79 infants). During the study period (see below), 102 infants were born. Nine of them died shortly after birth and were not included in the study. Hence, the infant sample used to assess dyadic male– infant interactions consists of 93 infants (45 males and 48 females). Three of these infants died during their first year of life. Behavioural Observations Male–infant interactions Data on dyadic male–infant interactions come from three sources. (1) Long-term ad libitum observations (see also Taub 1980b) on male–infant associations of 65 infants born in group C between 1985 and 1987. These observations were conducted almost daily from the day of birth until the end of the first year of life. During this period 2149 male–infant handling episodes were recorded. (2) Systematic time sampling (Martin & Bateson 1986) of 28 infants born in three social groups (B, C, F) between March and June 1988. Infants were observed from the day of birth until approximately 6 (groups B and F) or 9 (group C) months of age; one infant died at the age of 1 month, another at 5 months. Since the observational conditions as well as the size of the groups did not allow conventional scan sampling procedures, we used an alternative instantaneous sampling technique. All infants of each group were searched for and scored in rapid succession. At least 30 min elapsed between successive observations of the same infant. During each score, the behaviour of the infant, the behaviour and identity of its contact partner (if present), the identity of all animals within 1 m, and supplementary notes were recorded. Each subject was scored

157

approximately 80–100 times per month, totalling 15 061 scores or sample points (on average 604 per individual in group C, and 472 in groups B and F). During this period 1540 male–infant handling episodes were recorded. Since recording rules did not include continuous sampling, only behavioural states (sensu Altmann 1974) were recorded. General terms such as ‘infant handling’ or ‘male care’, therefore, refer to friendly forms of close body contact (grooming, carrying, huddling). To correct for differential observation time within groups, individual infant handling rates (number of infant handling episodes per male divided by all observed male infant handling episodes in the respective group#100) were calculated. (3) Continuous focal animal sampling of 16 adult and subadult males during 1 year in group C (see below). Behavioural states such as time spent with infants were recorded by 1-min instantaneous sampling. Analysis of ‘preferential male–infant relationships’ was restricted to males moderately to heavily involved with infants. Males were ‘heavily involved’ whenever their number of infant handling episodes was at least the mean plus one standard deviation of all adult and subadult males of the respective group and year. Individuals with values ¢X" Y  but below X+1  were ‘moderately often involved’. Males that did not reach this value were termed ‘rare caretakers’, and infants that did not reach the respective value were ‘ignored infants’. Preferential relationships refer to ‘primary’ and ‘secondary’ infants of a given male. The infant a male most often associated with, and those that received at least 51% of the attention given to the most favoured infant, were termed ‘primary’ infants. Infants that received between 50 and 33% of the attention that a male showed to his most favoured infant were termed ‘secondary’ infants (cf. Taub 1984). The analysis of triadic male–infant interactions (see Deag 1980, for a general description) was based on continuous focal male sampling protocols in one group (C) during 1 year (1986). The group consisted of 33 adult and subadult males and 24 infants. All males aged 6 years and older (N=16, all non-natal) were chosen as focal subjects. For each male there were 36 10-min observation sessions, resulting in 576 male sessions and 96 h of observation, respectively. The sessions of each male were equally distributed between the early morning before the monkeys were

158

Animal Behaviour, 51, 1

provisioned by the animal keepers (usually at about 0900 hours), the ‘non-feeding situation’, and during or up to 1 h after the monkeys were provisioned, the ‘feeding situation’. Sexual interactions and male reproductive success To test predictions of the mating effort hypothesis, we analysed data on mating activities of group C mothers during the mating season following the birth of their infants and data on paternity of infants sired in that season. Only mothers of infants that received care from males (infants moderately to heavily involved with males, number of infant handling episodes ¢X" Y ) were considered. Identity of caretakers (‘primary’ and ‘secondary’ males, defined as above) was viewed from the infants’ perspective. Data on mating activities were recorded almost daily during all four mating seasons (1985–1986 to 1988–1989) using ad libitum sampling (see Paul et al. 1993). Mating activity refers to all observed copulations and consort bouts (close associations, such as grooming or huddling contacts) between a given sexually mature male and oestrous females during the whole mating season, regardless of whether conception occurred in these oestrous periods. If two ejaculatory copulations occurred within one bout, this was counted as two bouts. Since sexual interactions between familiar maternal relatives are strongly avoided (Paul & Kuester 1985; Kuester et al. 1994), such dyads were excluded from the analysis. Data on male care and subsequent mating success were available for 32 mother–infant pairs (1023 observed mating bouts, X&= 32.0&21.68; seven females with fewer than five observed contacts excluded), and data on male care and paternity of the next sibling were available for 16 infant–infant pairs with a 1-year birth interval and four additional pairs with a 2-year birth interval.

rank of infants refers to the mother’s rank at birth. Paternity Determination Matrilineal kin relations of all infants were known from long-term observations on female reproductive history. For paternity analysis, we collected blood samples in autumn 1988 during routine captures from all individuals of the population. DNA was extracted using standard procedures (Maniatis et al. 1982) and digested with three restriction enzymes (Alu I, Hae III and Hinf I). Gels were successively hybridized with six synthetic ‘simple repeat’ oligonucleotide probes: [GTG]5, [GACA]4, [GATA]5, [GA]8, [GT]8 and [GGAT]4 (see Epplen et al. 1991, for a review of the oligonucleotide fingerprint technique). For each infant, its mother and potential fathers, 15 enzyme/probe combinations were used during analysis (see Kuester et al. 1992, for further details). Variable banding patterns were obtained with all probes, and paternal specific bands (10.6 on average: Kuester et al., in press) occurred in all infants. Nevertheless, exclusion of all potential fathers except one (the actual father) was not possible for eight out of the 91 infants available of the present sample. In these cases, two to three males remained as potential fathers. Since none of these males cared for its putative offspring, the analysis on male care and paternity was not affected, however. Two infants were sired by an extra-group male, and three additional infants of non-natal females were sired by males from other groups. In one case the father immigrated into the group the infant lived in and was therefore a potential caretaker.

RESULTS Dyadic Male–Infant Interactions Involvement of males and infants

Rank relations Rank relations of males and females were determined by the outcome of dyadic agonistic encounters and/or approach–retreat interactions. For analytical purposes, both the male and the female hierarchy were divided into a high-ranking class and a low-ranking class of equal sizes. Maternal

The frequency of male–infant handling episodes was strongly dependent on male age. Juvenile males and adolescent 4-year-old males handled infants less often than expected from their relative representation in the population, while males of all other ages handled infants more frequently than expected (Fig. 1). Males aged 6 years and older showed significantly higher rates of infant

Paul et al.: Male–infant interactions in macaques 350

Expected Observed

Number of episodes

300 250 200 150 100 50 0

1

2

3

4

5 6 7 8 Age (years)

9 10 11 12+

Figure 1. Frequency of male–infant handling episodes in relation to male age. Database: groups B, C, F (1988); N=144 males, 1540 observed episodes.

handling (X&=4.4&3.41, N=59) than did younger males (0.5&1.14, N=85; Mann–Whitney U=423.5, P<0.001). A comparison of recent immigrants and long-term residents of similar ages, possible in one group only (F), revealed no differences in infant handling frequency between them (U=29.0, N1 =9, N2 =7, P=0.78). The focal-male data revealed that males (aged 6 years and older) spent on average 9.3% of the observation time in close body contact with infants (range: 2.5–19.3%, =4.40, N=16). There was no significant correlation between male dominance rank and time spent with infants in this sample (rS = "0.33, N=16, P>0.10). In all three groups (6 group-years with 170 adult and subadult male years), 32 males (18.8%) were heavily involved with infants, 71 (41.8%) were moderately often observed in contact with infants, and 67 males (39.4%) were rare caretakers. Most heavily involved males were adult (27 out of 84 adult males versus 5 out of 86 subadult males) and high ranking (27 out of 84 high-ranking males versus 5 out of 86 low-ranking males; note that the high- and low-ranking samples are largely but not completely identical with the adult and subadult male classes). Topranking males were moderately involved in all cases. Nearly one half (42/93) of the infants were ignored by males; 21 of them were never seen in contact with males. Both sex and maternal rank appeared to influence the attractiveness of infants: female infants were more often ignored than male

159

infants (27 out of 48, or 56.3%, versus 15 out of 45, or 33.3%; ÷2 =4.04, df=1, P<0.05); and lowborn infants were much more often ignored than high-born ones (27 out of 44, or 61.4%, versus 15 out of 49, or 30.6%; ÷2 =7.65, df=1, P<0.01). Individual male preferences (comparing the number of infant handling episodes in each group and year per the number of infants available in the respective class) yielded the same result, but if the tests were performed independently for adult and subadult males, different patterns emerged (Table I): adult males preferred high-born infants (irrespective of the infants’ sex), while subadult males preferred male infants (irrespective of their mothers’ rank). Genetic relatedness and male–infant preferences Neither adult nor subadult males biased their caretaking activities towards related infants (Table II). Fathers cared for their own progeny as often as expected by chance. A goodness-of-fit test using three categories of genetic relatedness (fathers, maternal kin, unrelated dyads) yielded a non-significant result (÷2 =2.52, df=2, P>0.20). The results also indicate that siblings were not preferred over unrelated infants (÷2 =0.46, df=1, P=0.50; but note that in this case the formal criteria for a chi-squared statistic were not met because one expected value was less than 5). Reproductive Success of Caretakers The mating effort hypothesis predicts (1) that caretakers should be preferred mating partners of the infant’s mother during the mating season following the birth of the infant and (2) that they should ultimately have a greater probability of siring the next offspring of the mother than non-caretakers. To test the first prediction, we examined whether caretakers were also the most successful mating partners of the mother (in both cases ‘primary and secondary males’). The analysis revealed that caretakers were successful mating partners in 20 out of 79 possible dyads (25.3%), while non-caretakers were successful in 153 out of 816 possible dyads (18.8%; ÷2 =1.59, df=1, P>0.20). Since adult males acted more often as caretakers and achieved a higher general mating and reproductive success than subadult males, the analysis was repeated for this age class only. Now

Animal Behaviour, 51, 1

160

Table I. Number of infant handling episodes in relation to male age class, infant sex and maternal rank

Male category

Infant class

Episodes per infant (X&)

All mature males

Male Female High-born Low-born Male Female High-born Low-born Male Female High-born Low-born

2.2&3.16 0.8&1.42 2.0&2.42 1.1&2.03 2.5&3.60 1.6&1.68 3.1&2.76 1.1&2.10 1.8&2.59 0.1&0.34 0.9&1.36 1.0&1.96

Adult males

Subadult males

Wilcoxon T

P

2990.5

<0.001

4501.0

<0.001

1245.5

>0.30

735.0

<0.001

97.0

<0.001

1773.0

>0.60

Maternal rank: N=170 male-years. Infant sex: N=150 male-years (group F, where only female infants were available, excluded).

Table II. Genetic relatedness and preferential male–infant dyads of males moderately to heavily involved with infants Adult males

Type of dyad Father–offspring (r=0.5) Sibling–sibling† (r=0.25) Uncle–nephew/niece† Nephew–uncle/aunt (r=0.125) Cousin–cousin† (r=0.625) Other maternal kin Unrelated

No. of dyads possible

Subadult males

Preferential relationships Observed

Expected

No. of dyads possible

Preferential relationships Observed

Expected

83

7*

7.39

6

0

0.23

4

1

0.36

32

3

1.22

9

0

0.80

44

0

1.67

1

0

0.09

43

1

1.63

3 1313

0 118

0.27 116.86

13 1230

0 48

0.49 46.74

Database: group B: 1988, 8 infants; group C: 1985–1988, 79 infants; group F: 1988, 6 infants; note that four infants were sired by non-group males. *Conservative measure, assuming that one infant which was carried by several males, but was not available for paternity testing, had a special relationship with its father. †Matrilineal kin only.

the relation reversed: 12 out of 54 caretakers (22.2%), but 83 out of 281 non-caretakers (29.5%) were the most successful mating partners of the infants’ mothers (÷2 =0.86, df=1, P>0.30; females whose infants did not receive care from adult males excluded). Since male care may not be the only criterion by which females choose a male as a mating partner,

a somewhat weaker prediction was also tested: caretakers should achieve an above average mating success with the infant’s mother more often than non-caretakers. The results of this analysis revealed that by this criterion caretakers were indeed more successful than non-caretakers (35 out of 79, 44.3%, versus 210 out of 816, 25.7%, ÷2 =11.57, df=1, P<0.001). However, the

Paul et al.: Male–infant interactions in macaques relationship ceased when only adult males were considered: adult caretakers achieved an above average mating success in 17 out of 54 possible cases (31.5%), non-caretakers in 90 out of 281 cases (32.0%, ÷2 =0.01, df=1, P>0.90). To test the second prediction, we analysed whether caretakers had a higher probability of siring the subsequently born sibling of their preferred infant than other males. Two of the 16 infants born after a 1-year birth interval were sired by caretakers of their earlier born sibling (N=84 caretaker–infant dyads), the other 14 by noncaretakers (N=364 dyads). All of the four infants born after a 2-year birth interval were sired by non-caretakers of their older siblings (N=114 dyads), while all seven caretakers were unsuccessful. Thus, only a minority of infants (10.0%) was sired by caretakers of previously born siblings, and caretakers were not more successful than non-caretakers (2.2% versus 3.8%). In both cases where caretakers sired the next sibling, caretakers represented a rather large proportion of all possible sires (28.6% and 17.9%), while in the other cases the number of caretakers among the potential sires was much lower (less than 10%).

161

Dominance rank of males correlated neither with the number of triadic interactions received (rS =0.26, N=16, P>0.30) nor with the number of triadic interactions initiated (rS = "0.15, N=16, P>0.5). The majority of carrier-initiated interactions (74 out of 92) were initiated by the subordinate male (binomial z= "5.73, two-tailed P<0.0001). Non-carrier-initiated interactions were initiated as often by subordinate males (N=48) as by dominant males (N=43). The pattern of both types of triadic interactions was significantly affected by the rank distance between participants. Males with a small rank distance, i.e. males of adjacent or nearly adjacent rank, interacted more frequently than expected by chance with each other, while males with a large rank distance interacted less frequently than expected (Fig. 2). Similarly, triadic interactions were observed in a significantly larger proportion of dyads with a small rank distance (Table III). Only 10 out of the 193 triadic interactions were preceded by an aggressive encounter between the participants. Moreover, in four of these cases the interaction was initiated by the aggressor. Thus, very few triadic interactions could be classified as a response to aggression.

Triadic Male–Infant Interactions During focal observations 193 triadic male– male interactions were recorded. Two further interactions occurred between a mother and a male carrying her infant. In 19 additional cases approaches of carriers were terminated by an aggressive response from the higher-ranking opponent. In the majority of triadic male–male interactions (N=185) infants were used, in the remaining cases yearlings and 2 year olds were involved. During most interactions (N=185), males established body contact with each other, in the remaining eight cases males teeth-chattered but were close to each other. Focal males initiated on average 1.0 triadic interaction per h (=0.53), and they also received 1.0 interaction per h (=0.54). There was a significant correlation between the amount of time males spent in physical contact with infants and the frequency of triadic interactions they initiated as carriers (rS =0.74, N=16, P<0.01). There was no significant correlation, however, between contact time with infants and being a recipient of triadic interactions initiated by non-carriers (rS =0.38, N=16, P>0.10).

Relationships between infants, carriers and opponents In only a small minority (N=15) of triadic male–infant interactions with known kin relations between males and infants (N=180) was either the carrier or his opponent a relative of the infant (Table IV). In no case were both males related to the infant. As might be expected, carriers had a caretaking relationship with the infant used in most interactions (69 of 88, or 78.4% of carrier-initiated interactions, and 72 of 91, or 79.1% of noncarrier-initiated interactions; see Table IV). Remarkably often, however, caretakers were also recipients of carrier-initiated interactions (47 out of 88 episodes). To test whether this represented a deviation from a chance distribution, we compared the number of observed caretaker and noncaretaker dyads with those possible (only males aged 6 years and older were considered, since younger males were recipients in only two cases). Since there were 232 possible caretaker dyads, but 1088 possible non-caretaker dyads, the observed values differ significantly from those expected

Animal Behaviour, 51, 1

162 35

Expected Observed

Number of episodes

30 25 20 15 10 5 0

1

2

3

4 5 6 7 8 Rank distance

9 10 11 12 13 14 15

Figure 2. Frequency of triadic male–infant interactions in relation to rank distance between males (chi-squared goodness-of-fit=48.23, combining rank distances 12–15, df=11, P<0.001; N=161 interactions between focal males; see Table III for statistically independent data).

Table III. Occurrence of triadic interactions within male–male dyads of different rank distances* Triadic interactions Rank distance

Observed

Not observed

Total

1–3 4–8 9–15 Total

31 23 6 60

11 27 22 60

42 50 28 120

*÷2 =18.98, df=2, P<0.001.

(caretakers observed: N=47, expected: 15.5; noncaretakers observed: N=41, expected: 72.9; ÷2 =77.98, df=1, P<0.001). Nevertheless, triads in which both males shared a common caretaking relationship with the infant were not the norm (34 of 88 carrier-initiated interactions, and 35 of 91 non-carrier-initiated interactions). Interactions in which none of the males had a caretaking relationship with the infant they used were extremely rare (6 of 88 carrier-initiated interactions, 0 of 91 non-carrier-initiated interactions). Male–male grooming Only a minority of triadic interactions (22 out of 193) were followed by grooming between the males. Nevertheless, the presence of an infant

seemed to facilitate grooming interactions between adult (and subadult) males. Of 52 observed grooming episodes between adult and/or subadult males (one interaction with a juvenile excluded), 21 occurred after a triadic interaction. Eight grooming episodes (15.4%) were initiated without the presence of an infant. In 23 further episodes, the start of the interaction was not observed. In nine of these, an infant was present (in one case a yearling) at the start of the observation session. In the other 14 cases, no infant was present (but probably was before, at least in some cases, since infants often leave males after triadic interactions). Almost all grooming between males was directed towards the higher-ranking male (50 out of 52 episodes; in the remaining two cases the males were rank neighbours). Only three episodes, all after a triadic interaction, were observed between adult males. Adult males never groomed subadults, while subadult males groomed adults on 31 occasions, and males of their own age class on 18 occasions. A comparison between expected and observed number of grooming dyads revealed that adult males groomed each other less often than expected (2 observed dyads, 5.8 expected, N=55 possible dyads), while the observed values were higher than those expected among other classes (subadult–adult: 26 dyads observed, 25.4 expected, N=242; subadult–subadult: 13 dyads

Paul et al.: Male–infant interactions in macaques

163

Table IV. Genetic and social relationships between infants, carriers and opponents Number of episodes Carrier-initiated

Genetic Father Maternal relative Unrelated Unknown Social Caretaker Non-caretaker Unknown Total

Non-carrier-initiated

Actor

Recipient

Actor

Recipient

0 1 88 3

3 0 86 3

5 4 82 0

3 0 88 0

69 19 4

47 41 4

54 37 0

72 19 0

92

91

Table V. Comparison of focal male interactions during the non-feeding and the feeding situation

Category

Non-feeding situation (X&)

Feeding situation (X&)

Wilcoxon T

P

Aggression total (N/h) Aggression between mature males (N/h) Time with infant (% sample points) Infant contact bouts (N/h) Triadic interactions (N/h) Grooming bouts with non-infants (N/h)

1.3&0.78 0.6&0.51 4.4&3.38 1.1&0.64 1.4&0.76 1.2&0.70

4.2&1.87 2.8&1.79 6.7&4.24 2.1&1.22 2.6&1.80 0.7&0.49

0 0 43.5 21.0 25.0 28.5

<0.001 <0.001  <0.02 <0.03 <0.04

observed, 10.0 expected, N=95). This bias did not reach statistical significance, however (÷2 =3.40, df=2, P>0.10).

aggressive response from the higher-ranking male occurred during the feeding situation. DISCUSSION

Context dependency of male–infant interactions As might be expected, during the feeding situation the focal males were significantly more often involved in agonistic interactions with other individuals, including adult and subadult males (Table V). Total contact time with infants did not increase significantly during the feeding situation, but the frequency of contact bouts did, indicating that males more often established contact with infants during the feeding situation. Grooming interactions with other (non-infant) individuals decreased, but the frequency of triadic male– infant interactions increased significantly from, on average, 1.4 to 2.6 interactions per h. Moreover, almost all carrier-initiated approaches of males (16 out of 19) that were terminated by an

The Paternal Investment Hypothesis Our data clearly do not support earlier suggestions (Taub 1984, 1985, 1990; Taub & Mehlman 1991) that kinship is the ‘primary underpinning’ of male–infant interactions in Barbary macaques. While all males showed strong preferences for specific infants, neither adult nor subadult males biased their ‘caretaking activities’ towards maternally or paternally related infants. This observation is consistent with earlier findings in the same population (Paul 1984; Kuester & Paul 1986) and with results from a study on wild Algerian Barbary macaques (Ménard et al. 1992). In Ménard et al.’s (1992) study, where (incomplete) genetic paternity analyses were undertaken,

164

Animal Behaviour, 51, 1

the single identified father did not carry his offspring but infants he had not sired, as did several other males. Nevertheless, Ménard and coworkers still felt it possible ‘that paternity is one of the factors influencing male investment’ (1992, page 171). The data presented here and in an earlier report (Paul et al. 1992) clearly do not support this hypothesis. Paul et al. (1992) suggested that the fact that males did not prefer to associate with their own progeny (a finding confirmed by this larger sample) indicates that males are not able to recognize their offspring (e.g. via phenotype matching). Obviously, however, this is not the only possible explanation: males could simply have other preferences. Our observation that males (in striking contrast to females; A. Paul & J. Kuester, unpublished data) did not even prefer maternal siblings over unrelated infants supports this interpretation. In Kuester & Paul’s (1986) study, some young subadult males preferred infants of their own matriline in one year but not in another. This also indicates that kinship is much less important than other infant characteristics, such as gender and maternal rank. Nevertheless, the hypothesis that Barbary macaques are not able to recognize paternal kin via phenotype matching (see also Fredrickson & Sackett 1984; Sackett & Fredrickson 1987) is strongly supported by the finding that incestuous matings are avoided between maternal kin but not between paternal kin (Paul & Kuester 1985; Kuester et al. 1994; see also Smith 1986, for rhesus monkeys, M. mulatta; Inoue et al. 1990, for Japanese macaques, M. fuscata). Given the promiscuous nature of the mating system of Barbary macaques (Taub 1980a; Small 1990; Kuester & Paul 1992), it is not surprising that males have no cues to recognize their progeny. It might be possible, however, that caretakers are, on average, more likely to be fathers than non-caretakers, based on their general mating success. Adult males of this study handled infants more often than subadult males (a finding contrasting with the results of Taub 1984), which could be taken as evidence in support of this hypothesis, since adult males had a much higher mating and reproductive success than subadult males (see Paul et al. 1993). The behaviour of recent immigrants, which handled infants no less frequently than residents, does not contradict this, since all these males had some (albeit few)

opportunities to mate with females of their new group. Moreover, the only male that immigrated after the end of the mating season (not included in the quantitative analysis presented in the Results) rarely carried infants conceived in that season. However, Paul (1984) found strong affiliations between infants and recent immigrants that were sexually immature at the time of immigration. Moreover, although subadult males as a group carried infants less frequently than adult males in this study, several of them developed strong bonds with unrelated infants despite a low (often zero) mating success. It seems unlikely, therefore, that the males’ overall paternity chances affected their caretaking motivation. It also seems unlikely that females mate promiscuously with all males in order to induce care from almost all males (Taub 1980a; Busse 1985; Hrdy 1986). There are three lines of evidence against this ‘paternity confusion’ hypothesis. First, virtually all studies (including Taub’s own study) revealed that males show striking preferences for specific infants and ignore all others (Deag 1974, 1980; Taub 1978, 1984; Paul 1984; Kuester & Paul 1986; Ménard et al. 1992; Paul et al. 1992). The paternity confusion hypothesis does not predict this specificity. Second, several studies showed that a large proportion of available infants were ignored by all males (11 of 39: Ménard et al. 1992; 14 of 36: Paul 1984; 42 of 93: this study; 1 of 5: Taub 1984), although there is no evidence that the mothers of these infants mated at a lower rate than mothers of non-ignored infants. Third, as Kurland & Gaulin (1984) noted, even if males care indiscriminately for infants, and if infants benefit from male care, this could only alter their absolute, but not their relative fitness. It should be noted that these arguments do not contradict Hrdy’s (1986) hypothesis that female promiscuity is a tactic to confuse paternity in order to prevent male infanticide. In summary, the paternity confusion hypothesis does not explain the highly differentiated male care system of Barbary macaques. Other predictions of the paternal investment hypothesis, for example improved survival, later status or reproductive success, have also not been substantiated by empirical data (Kuester & Paul 1986, 1988). A single death of an infant with no male caretakers (Taub 1978, 1980a, b, 1984) should not be taken as evidence that male care is necessary for infant survival. Neither should

Paul et al.: Male–infant interactions in macaques observations of ‘aunting to death’ (Hrdy 1976) by male Barbary macaques (Paul & Thommen 1984; Kuester & Paul 1986) be interpreted as evidence for infant abuse. In general, males treat infants carefully, and by far the majority of infants born in the Salem colony were not harmed by male care. Since infant mortality in the Salem Barbary macaque population is quite low (Paul & Kuester 1988), each single neonatal death from male ‘care’ and male restrictiveness necessarily represents a relatively high proportion of all infant deaths in that colony. Interestingly, at present, where only few infants are born because of large-scale birth control, cases of ‘allomothering to death’ are much more frequent (personal observation; W. Angst, personal communication). Cases of ‘allomothering to death’ are an indication, however, that males handle infants for their own and not the infant’s benefit. This view is supported by Paul’s (1984) observation that males were more responsible for maintaining contact with infants, and for longer, than mothers were. Maternal responsibility ended during the infants’ third month of life, but the males’ responsibility persisted until the end of the infants’ first year of life. Moreover, Timme (1993) found that frequent infant handling by males led to less nipple contact and, contrary to Burton’s (1972) assessment, a delay in infant independence. Thus, infant handling by males may be costly for infants and their mothers, who often make considerable efforts to retrieve their newborns (Paul 1984). Whether the paternal investment hypothesis is better suited to explain male–infant relations in other species living in multimale groups remains to be tested by genetic data. Some studies found strong inferential evidence for paternal investment in savanna baboons, Papio cynocephalus (Busse & Hamilton 1981 and, especially, Anderson 1992), while the results of others appear equivocal (Packer 1980; Stein 1984; Strum 1984; Smuts 1985; Collins 1986). Protectiveness and/or affiliation of older and previously high-ranking males as a response to the threat of infanticide (Noë & Sluijter 1990, for savanna baboons; de Ruiter et al. 1994, for long-tailed macaques, M. fascicularis; Winkler et al. 1993, for Hanuman langurs, Presbytis entellus), may also be explained in the framework of paternal investment. In contrast to Barbary macaques, however, paternity certainty appears to be relatively high in these cases.

165

The Mating Effort Hypothesis At least among Old World primates, male– infant interactions are more common in species with a multimale breeding system and low paternity certainty than in one-male breeding systems (Smuts & Gubernick 1992; see also Stein & Stacey 1981). Since male–infant relations are often mediated by a special affiliation between the male and the infant’s mother (Busse 1985), it appears possible that males use infants to increase their access to the infant’s mother (Smuts 1985). Contrary to earlier speculations (Small 1990), special relationships or ‘friendships’ (Smuts 1985) between male and female Barbary macaques have been observed (Prud’homme 1991; Skamel & Paul 1994), although these relationships appear to be less intense than in baboons. While these friendships may sometimes be extended to the females’ infants (especially to infants of top-ranking females), such coincidences appear not to be the rule (Paul 1984). In Skamel & Paul’s study, none of the caretakers had a special relationship with the mother of their preferred infant (unpublished data). The present study shows that the mating effort hypothesis does not explain male–infant relations in Barbary macaques. Caretaking relationships enhanced neither the males’ chance of mating with the infants’ mothers nor their chance of siring the mother’s next offspring. Moreover, in contrast to Taub (1980a, page 297) we did not observe males ‘attracting’ oestrous females by ‘carrying an infant dorsally in clear view of the female’. In fact, male–infant interactions are strongly reduced during the mating season, especially among peripheralized males (Paul 1984). Although the controversial topic of female choice in non-human primates is beyond the scope of this paper, it should be noted that even in savanna baboons there is no unequivocal evidence that male care increases the chances that a male will mate with the infant’s mother when cycling resumes (Bercovitch 1991). Affiliative behaviour towards infants may increase a male’s chance of being tolerated by the mother (Keddy Hector et al. 1989; see also Ferrari 1992), but whether this results in higher reproductive success is unknown. Whether females select males as mating partners on the basis of their ‘male care qualities’ remains to be shown, therefore.

166

Animal Behaviour, 51, 1

The Agonistic Buffering Hypothesis The only hypothesis supported by this study was Deag & Crook’s (1971) agonistic buffering hypothesis. Males not only interacted with infants on a dyadic basis, they also used them in triadic interactions, and that in accordance with their availability. This behaviour is in sharp contrast to that of mothers, who are often recipients of triadic interactions, but almost never initiate such interactions as carriers (Paul 1984). As noted by Deag (1974, 1980) and Merz (1978), the infants’ role during these interactions is passive; occasionally, even dead infants are used (Merz 1978). Although Taub’s (1980b) reservation about the use of the term ‘agonistic buffering’ seems to be justified in so far as triadic interactions were rarely initiated as a response to aggression (see also Deag 1980), three lines of evidence support this hypothesis. First, at least in carrier-initiated triadic interactions, the subordinate male was much more likely to approach the dominant male than vice versa. The same pattern was found by Deag (1980: 51 out of 68 interactions), Paul (1984: 434/508) and Taub (1980b: 282/331; see also Silk & Samuels 1984 for bonnet macaques, M. radiata). Second, the fact that the increase in aggressive encounters during the ‘feeding situation’ led to a similar increase in male–infant contacts and triadic interactions but not to an increase in other affiliative interactions such as grooming suggests that inter-male tension is a causal factor underlying the males’ motivation to associate with infants (see also Strum 1984, for savanna baboons), and to use them in triadic interactions. And third, affiliative contacts (‘grooming’) between adult males were never observed outside the context of male–infant interactions. Thus, as Deag (1980, page 58) stated, ‘the presence of the baby appears essential’. Contrary to the prediction of the agonistic buffering hypothesis, in non-carrier-initiated interactions the approaching male was as often subordinate as dominant (see also Deag 1980; Taub 1980b; Paul 1984). In fact, Deag (1980, page 78) explicitly stated that such cases did not fit the hypothesis. Apparently, rank asymmetry alone does not govern the pattern of triadic interactions. However, contrary to Deag’s (1980, page 76) assumption, rank relations of adult Barbary macaque males are not at all ‘reasonably stable’ (Witt et al. 1981; Paul 1989; see also Table 1 in

Taub 1980b). Moreover, coalitionary attacks may override dyadic dominance relations (Kuester & Paul 1992). Thus, it might be beneficial to establish friendly relationships with closely ranked males, even if they are actually subordinate, because these males are either potentially the most dangerous competitors or the most beneficial allies (see below). The fact that triadic interactions were overrepresented between males with a small rank distance (see also Stein’s 1984 reanalysis of Taub’s data) supports this view. Although we concur with Taub’s (1980b) notion that the interacting males’ relationship with the infant is an important variable, his interpretation of triadic interactions was not supported. Taub suggested that the interacting males share a common interest (based on kinship ties) in the same infant, and that subadult males ‘tell’ adult males via triadic interactions ‘that they are both related to this particular infant’ (Taub 1984, page 53). Clearly, this interesting idea lacks any foundation. In none of the cases observed here were both of the males related to the infant, and in very few cases was one male a relative of the infant. This finding is also inconsistent with two versions of the agonistic buffering hypothesis, developed to explain similar triadic male–infant interactions in savanna baboons. Popp (1978) suggested that males carrying infants during triadic interactions are recent immigrants and unrelated to the infant, while opponents are likely to be fathers and thus reluctant to attack the carrier. Unfortunately, this elegant hypothesis was not confirmed by Popp’s own data and data from other studies (e.g. Busse & Hamilton 1981; Stein 1984; Collins 1986). Conversely, Busse & Hamilton (1981) suggested that carriers protect offspring against immigrant, potentially infanticidal males (see also Busse 1984). In Collins’ (1986) study, however, most interactions took place between resident males, and Packer & Pusey (1985) showed that carriers were likely to be fathers in only 40% of the observed cases. In the present study, both carriers and opponents were often likely to be fathers of the infant concerned, though rarely actual ones, and in Paul’s (1984) study a considerable proportion of triadic male– infant interactions (264 out of 1701, 15.5%) took place between recent immigrants, that is, they were unlikely to be fathers. Thus, the likelihood of paternity did not appear to affect the pattern of triadic interactions.

Paul et al.: Male–infant interactions in macaques Nevertheless, the observation that caretakers were preferred recipients of triadic interactions (see also Paul 1984) underlines the importance of the males’ relationship to the infant used. Males apparently know of the relationships between other group members (Cheney & Seyfarth 1990), and they use this knowledge in a sophisticated manner. It is widely accepted that familiarity reduces aggressiveness (e.g. Angst 1980), and it appears that males exploit this effect by carrying infants to males familiar with the infant (see also Ogawa 1995, for Tibetan macaques, M. thibetana). Since familiarity usually results from kinship or other beneficial relations, the inhibitory effect of familiar, but unrelated infants may well be a by-product of other selective pressures. That agonistic buffering works by an ‘innate releasing mechanism’ of the infants’ natal coat colour (‘Kindchenschema’: Lorenz 1943) seems rather unlikely. In Paul’s (1984) study, triadic interactions were not terminated after the infants had lost their natal coat colour, and in the present study occasionally yearlings and even 2 year olds were used, despite the large number of infants available (see also Stein 1984, for savanna baboons). Moreover, although infanticide has rarely been observed in Barbary macaques (Angst & Thommen 1977), natal coat colour does not protect infants from infanticidal males. It might also be that agonistic buffering works because other group members, including the infant’s mother and other relatives, might mob the aggressor if the interaction escalates and the infant shows signs of stress (Busse 1984; Dunbar 1984; Stein 1984; Collins 1986). This interpretation is supported by the fact that adult males prefer infants from high-ranking matrilines (see also Paul 1984; Kuester & Paul 1986), and that top-ranking females sometimes intervene in male disputes (personal observation). Obviously, however, the preference of subadult males for male infants, irrespective of maternal rank, requires another explanation. It is quite possible, however, that ‘agonistic buffering’ in its strict sense (inhibition of aggression) is not the only function of triadic male– infant interactions in Barbary macaques (see also Deag 1980). Stein (1984, page 186) suggested that in savanna baboons ‘by utilizing infants as buffers, males are able to interact with higherranking males more than they would otherwise be

167

able, thus establishing stronger bonds with those males’. In savanna baboons and chimpanzees, Pan troglodytes, coalitionary relationships between males apparently increase male mating opportunities and, presumably, reproductive success (Cheney et al. 1986). The same appears to be true for Barbary macaques (Kuester & Paul 1992). It seems likely, therefore, that triadic interactions also serve to establish coalitionary relationships between males. Both the observation that most triadic interactions could be classified as friendly approaches and that these interactions were most common between males with a small rank distance are consistent with this interpretation. Longitudinal data on male–male relationships are badly needed to test this hypothesis more rigorously. If it turns out to be true, however, that alliance formation and its presumed fitness effect is the ultimate goal of triadic interactions, then male– infant interactions among Barbary macaques can be considered as mating effort.

ACKNOWLEDGMENTS We are grateful to Gilbert de Turckheim, Ellen Merz and Walter Angst for their support of our work at Affenberg Salem and permission to take blood samples. We thank Carsten Botor, Elke Hertwig, Doris Podzuweit, Anne Steuckardt, Angelika Timme, Signe Preuschoft and Dorothea Wrogemann who contributed to data collection in group C, Jörg Epplen for introducing us to the oligonucleotide fingerprint technique, and the Institut für Humangenetik, the Institut für Rechtsmedizin and the Zentrales IsotopenLaboratorium, Universität Göttingen for logistical support. For discussions and/or comments we thank Silvana Borgognini Tarli, Robin Dunbar, Uta Skamel, Bernard Thierry, Eckart Voland and an anonymous referee. The study was financially supported by the Deutsche Forschungsgemeinschaft (grants An 131/1-6, Vo 124/15-1, 18-1, Pa 408/2-1). This paper is dedicated to the late Christian Vogel, without whose support and encouragement this research would not have been possible.

REFERENCES Altmann, J. 1974. Observational study of behavior: sampling methods. Behaviour, 49, 227–267.

168

Animal Behaviour, 51, 1

Anderson, C. M. 1992. Male investment under changing conditions among chacma baboons at Suikerbosrand. Am. J. phys. Anthropol., 87, 479–496. Angst, W. 1980. Aggression bei Affen und Menschen. Berlin: Springer-Verlag. Angst, W. & Thommen, D. 1977. New data and a discussion of infant killing in Old World monkeys and apes. Folia primatol., 27, 198–229. Bercovitch, F. B. 1991. Mate selection, consortship formation, and reproductive tactics in adult female savanna baboons. Primates, 32, 437–452. Burton, F. D. 1972. The integration of biology and behaviour in the socialization of Macaca sylvana of Gibraltar. In: Primate Socialization (Ed. by F. E. Poirier), pp. 26–62. New York: Random House. Busse, C. D. 1984. Triadic interactions among male and infant chacma baboons. In: Primate Paternalism (Ed. by D. M. Taub), pp. 186–212. New York: Van Nostrand Reinhold. Busse, C. D. 1985. Paternity recognition in multi-male primate groups. Am. Zool., 25, 873–881. Busse, C. D. & Hamilton, W. J., III. 1981. Infant carrying by male chacma baboons. Science, 212, 1281–1283. Cheney, D. L. & Seyfarth, R. M. 1990. How Monkeys See the World. Chicago: University of Chicago Press. Cheney, D. L., Seyfarth, R. M. & Smuts, B. B. 1986. Social relationships and social cognition in nonhuman primates. Science, 234, 1361–1366. Clutton-Brock, T. H. 1991. The Evolution of Parental Care. Princeton, New Jersey: Princeton University Press. Collins, D. A. 1986. Interactions between adult male and infant yellow baboons (Papio c. cynocephalus) in Tanzania. Anim. Behav., 34, 430–443. Deag, J. M. 1974. A study of the social behaviour and ecology of the wild Barbary macaque Macaca sylvanus L. Ph.D. thesis, University of Bristol. Deag, J. M. 1980. Interactions between males and unweaned Barbary macaques: testing the agonistic buffering hypothesis. Behaviour, 75, 54–81. Deag, J. M. & Crook, J. H. 1971. Social behaviour and ‘agonistic buffering’ in the wild Barbary macaque Macaca sylvana L. Folia primatol., 15, 183–200. Dunbar, R. I. M. 1984. Infant-use by male gelada in agonistic contexts: agonistic buffering, progeny protection or soliciting support? Primates, 25, 28–35. Epplen, J. T., Ammer, H., Epplen, C., Kammerbauer, C., Mitreiter, R., Roewer, L., Schwaiger, W., Steimle, V., Zischler, H., Albert, E., Andreas, A., Beyermann, B., Meyer, W., Buitkamp, J., Nanda, I., Schmid, M., Nürnberg, P., Pena, S. D. J., Pöche, H., Sprecher, W., Schartl, M., Weising, K. & Yassouridis, A. 1991. Oligonucleotide fingerprinting using simple repeat motifs: a convenient, ubiquitously applicable method to detect hypervariability for multiple purposes. In: DNA Fingerprinting: Approaches and Applications (Ed. by T. Burke, G. Dolf, A. J. Jeffreys & R. Wolff), pp. 50–69. Basel: Birkhäuser. Ferrari, S. F. 1992. The care of infants in a wild marmoset (Callithrix flaviceps) group. Am. J. Primatol., 26, 109–118.

Fredrickson, W. T. & Sackett, G. P. 1984. Kin preferences in primates (Macaca nemestrina): relatedness or familiarity? J. comp. Psychol., 98, 29–34. Hrdy, S. B. 1976. Care and exploitation of nonhuman primate infants by conspecifics other than the mother. In: Advances in the Study of Behavior, Vol 6 (Ed. by J. S. Rosenblatt, R. A. Hinde, E. Shaw & C. Beer), pp. 101–158. New York: Academic Press. Hrdy, S. B. 1986. Empathy, polyandry, and the myth of the coy female. In: Feminist Approaches to Science (Ed. by R. Bleier), pp. 119–146. New York: Pergamon. Inoue, M., Takenaka, A., Tanaka, S., Kominami, R. & Takenaka, O. 1990. Paternity discrimination in a Japanese macaque group by DNA fingerprinting. Primates, 31, 563–570. Itani, J. 1959. Paternal care in the wild Japanese monkey, Macaca fuscata. Primates, 2, 61–93. Keddy Hector, A. C., Seyfarth, R. M. & Raleigh, M. J. 1989. Male parental care, female choice and the effect of an audience in vervet monkeys. Anim. Behav., 38, 262–271. Kleiman, D. G. & Malcolm, J. R. 1981. The evolution of male parental investment in mammals. In: Parental Care in Mammals (Ed. by D. J. Gubernick & P. H. Klopfer), pp. 347–387. New York: Plenum Press. Kuester, J. & Paul, A. 1986. Male–infant relationships in semifree-ranging Barbary macaques (Macaca sylvanus) of Affenberg Salem/FRG: testing the ‘male care’ hypothesis. Am. J. Primatol., 10, 315–327. Kuester, J. & Paul, A. 1988. Rank relations of juvenile and subadult natal males of Barbary macaques (Macaca sylvanus) at Affenberg Salem. Folia primatol., 51, 33–44. Kuester, J. & Paul, A. 1992. Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour, 120, 192–217. Kuester, J., Paul, A. & Arnemann, J. 1992. Paternity determination by oligonucleotide DNA fingerprinting in Barbary macaques (Macaca sylvanus). In: Paternity in Primates: Genetic Tests and Theories (Ed. by R. D. Martin, A. F. Dixson & E. J. Wickings), pp. 141–154. Basel: Karger. Kuester, J., Paul, A. & Arnemann, J. 1994. Kinship, familiarity and mating avoidance in Barbary macaques, Macaca sylvanus. Anim. Behav., 48, 1183–1194. Kuester, J., Paul, A. & Arnemann, J. In press. Age, sex and individual differences of reproductive success in Barbary macaques (Macaca sylvanus). Primates. Kummer, H. 1967. Tripartite relations in hamadryas baboons. In: Social Communication among Primates (Ed. by S. A. Altmann), pp. 63–71. Chicago: University of Chicago Press. Kurland, J. A. & Gaulin, S. J. C. 1984. The evolution of male parental investment: effects of genetic relatedness and feeding ecology on the allocation of reproductive effort. In: Primate Paternalism (Ed. by D. M. Taub), pp. 259–308. New York: Van Nostrand Reinhold. Lorenz, K. 1943. U } ber die angeborenen Formen möglicher Erfahrung. Z. Tierpsychol., 5, 235–409.

Paul et al.: Male–infant interactions in macaques Maniatis, T., Fritsch, E. F. & Sambrook, J. 1982. Molecular Cloning. New York: Cold Spring Harbour. Martin, P. & Bateson, P. 1986. Measuring Behaviour. Cambridge: Cambridge University Press. Ménard, N., Scheffrahn, W., Vallet, D., Zidane, C. & Reber, C. 1992. Application of blood protein electrophoresis and DNA fingerprinting to the analysis of paternity and social characteristics of wild Barbary macaques. In: Paternity in Primates: Genetic Tests and Theories (Ed. by R. D. Martin, A. F. Dixson & E. J. Wickings), pp. 155–174. Basel: Karger. Merz, E. 1978. Male–male interactions with dead infants in Macaca sylvanus. Primates, 19, 749–754. Noë, R. & Sluijter, A. A. 1990. Reproductive tactics of male savanna baboons. Behaviour, 113, 117–170. Ogawa, H. 1995. Recognition of social relationships in bridging behavior among Tibetan macaques (Macaca thibetana). Am. J. Primatol., 35, 305–310. Packer, C. 1980. Male care and exploitation of infants in Papio anubis. Anim. Behav., 28, 512–520. Packer, C. & Pusey, A. 1985. Asymmetric contests in mammals: respect, manipulation and age-specific aspects. In: Evolution. Essays in Honour of John Maynard Smith (Ed. by P. J. Greenwood, P. H. Harvey & M. Slatkin), pp. 173–186. Cambridge: Cambridge University Press. Paul, A. 1984. Zur Sozialstruktur und Sozialisation semi-freilebender Berberaffen (Macaca sylvanus L. 1758). Ph.D. thesis, University of Kiel. Paul, A. 1989. Determinants of male mating success in a large group of Barbary macaques (Macaca sylvanus) at Affenberg Salem. Primates, 30, 461–476. Paul, A. & Kuester, J. 1985. Intergroup transfer and incest avoidance in semifree-ranging Barbary macaques (Macaca sylvanus) at Salem (FRG). Am. J. Primatol., 8, 317–322. Paul, A. & Kuester, J. 1988. Life-history patterns of Barbary macaques (Macaca sylvanus) at Affenberg Salem. In: Ecology and Behavior of Food-enhanced Primate Groups (Ed. by J. E. Fa & C. H. Southwick), pp. 199–228. New York: Alan R. Liss. Paul, A., Kuester, J. & Arnemann, J. 1992. DNA fingerprinting reveals that infant care by male Barbary macaques (Macaca sylvanus) is not paternal investment. Folia primatol., 58, 93–98. Paul, A., Kuester, J., Timme, A. & Arnemann, J. 1993. The association between rank, mating effort and reproductive success in male Barbary macaques (Macaca sylvanus). Primates, 30, 461–476. Paul, A. & Thommen, D. 1984. Timing of birth, female reproductive success and infant sex ratio in semifreeranging Barbary macaques (Macaca sylvanus). Folia primatol., 42, 2–16. Popp, J. L. 1978. Male baboons and evolutionary principles. Ph.D. thesis, Harvard University. Prud’homme, J. 1991. Group fission in a semifreeranging population of Barbary macaques (Macaca sylvanus). Primates, 32, 9–22. Ridley, M. 1978. Paternal care. Anim. Behav., 26, 904–932.

169

de Ruiter, J. R., van Hoof, J. A. R. A. M. & Scheffrahn, W. 1994. Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour, 129, 203–224. Sackett, G. P. & Fredrickson, W. T. 1987. Social preferences by pigtail macaques: familiarity versus degree and type of kinship. Anim. Behav., 35, 603–607. Silk, J. B. & Samuels, A. 1984. Triadic interactions among Macaca radiata: passports and buffers. Am. J. Primatol., 6, 373–376. Skamel, U. & Paul, A. 1994. Promiskuität und Freundschaft: Männchen-Weibchen-Beziehungen bei Berberaffen (Macaca sylvanus). In: Deutsche Gesellschaft für Säugetierkunde, 68. Hauptversammlung (Ed. by F. Spitzenberger & H. G. Erkert), page 41. Hamburg: Parey. Small, M. F. 1990. Promiscuity in Barbary macaques (Macaca sylvanus). Am. J. Primatol., 20, 267–282. Smith, D. G. 1986. Incidence and consequences of inbreeding in three captive groups of rhesus macaques (Macaca mulatta). In: Primates. The Road to SelfSustaining Populations (Ed. by K. Benirschke), pp. 856–874. New York: Springer. Smith, E. O. & Pfeffer-Smith, P. G. 1982. Triadic interactions in captive Barbary macaques (Macaca sylvanus, Linnaeus, 1758): ‘agonistic buffering’? Am. J. Primatol., 2, 99–107. Smuts, B. B. 1985. Sex and Friendship in Baboons. New York: Aldine. Smuts, B. B. & Gubernick, D. J. 1992. Male–infant relationships in nonhuman primates: paternal investment or mating effort? In: Father–Child Relations. Cultural and Biosocial Contexts (Ed. by B. Hewlett), pp. 1–30. Hawthorne, New York: Aldine. Stein, D. M. 1984. The Sociobiology of Infant and Adult Male Baboons. Norwood, New Jersey: Ablex. Stein, D. M. & Stacey, P. B. 1981. A comparison of infant–adult male relations in a one-male group with those in a multi-male group for yellow baboons (Papio cynocephalus). Folia primatol., 36, 264–276. Strum, S. C. 1984. Why males use infants. In: Primate Paternalism (Ed. by D. M. Taub), pp. 146–185. New York: Van Nostrand Reinhold. Taub, D. M. 1978. Aspects of the biology of the wild Barbary macaque (Primates, Cercopithecinae, Macaca sylvanus L. 1758): biogeography, the mating system and male infant associations. Ph.D. thesis, University of California, Davis. Taub, D. M. 1980a. Female choice and mating strategies among wild Barbary macaques (Macaca sylvanus). In: The Macaques: Studies in Ecology, Behavior and Evolution (Ed. by D. G. Lindburg), pp. 287–344. New York: Van Nostrand Reinhold. Taub, D. M. 1980b. Testing the ‘agonistic buffering’ hypothesis. I. The dynamics of participation in the triadic interaction. Behav. Ecol. Sociobiol., 6, 187–197. Taub, D. M. 1984. Male caretaking behavior among wild Barbary macaques (Macaca sylvanus). In: Primate Paternalism (Ed. by D. M. Taub), pp. 20–55. New York: Van Nostrand Reinhold. Taub, D. M. 1985. Male–infant interactions in baboons and macaques: a critique and reevaluation. Am. Zool., 25, 861–871.

170

Animal Behaviour, 51, 1

Taub, D. M. 1990. The functions of primate paternalism: a cross-species review. In: Pedophilia: Biosocial Dimensions (Ed. by J. R. Feierman), pp. 338–377. New York: Springer. Taub, D. M. & Mehlman, P. 1991. Primate paternalistic investment: a cross-species view. In: Understanding Behavior: What Primate Studies Tell Us About Human Behavior (Ed. by J. D. Loy & C. B. Peters), pp. 51–89. Oxford: Oxford University Press. Timme, A. 1993. Costs and benefits of male allomothering in Barbary macaque mother–infant pairs. Am. J. Primatol., 30, 351. Trivers, R. L. 1972. Parental investment and sexual selection. In: Sexual Selection and the Descent of Man, 1871–1971 (Ed. by B. Campbell), pp. 136–179. Chicago: Aldine. de Turckheim, G. & Merz, E. 1984. Breeding Barbary macaques in outdoor open enclosures. In: The Barbary Macaque: A Case Study in Conservation

(Ed. by J. E. Fa), pp. 241–261. New York: Plenum Press. Whitten, P. L. 1987. Infants and adult males. In: Primate Societies (Ed. by B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker), pp. 343–357. Chicago: University of Chicago Press. Winkler, P., Podzuweit, D. & Borries, C. 1993. Zur Toleranz gezwungen: oder warum Hanumanlanguren nicht nur in Harems leben. In: Evolution und Anpassung (Ed. by E. Voland), pp. 94–103. Stuttgart: S. Hirzel Verlag. Witt, R., Schmidt, C. & Schmitt, J. 1981. Social rank and Darwinian fitness in a multimale group of Barbary macaques (Macaca sylvana Linnaeus, 1758). Folia primatol., 36, 201–211. Woodroffe, R. & Vincent, A. 1994. Mother’s little helpers: patterns of male care in mammals. Trends Ecol. Evol., 9, 294–297.