Ethology 97, 47-64 (1994) 0 1994 Blackwell Wissenschafts-Verlag, Berlin ISSN 0179-1613

Departement d’tinthropologie, Universite de Montreal, Montreal

Effect of Male Competition on Male-Female Relationships in Bi-male Groups of Mountain Gorillas

PASCALE SICOTTE

SICOTTE, P. 1994: Effect of male competition on male-female relationships in bi-male groups of mountain gorillas. Ethology 97, 47-64.

Abstract

In gorillas (Gorilla gorilla beringei), male reproductive competition is manifested during inter- group encounters through displays and contact aggression with opposing males and through attempts to control the movement of females between groups. This paper documents the effect of within-group male reproductive competition on male-female relationships. In one-male groups, females are known to take the initiative in the maintenance of their relationships with males. In two-male units, because males face within-group reproductive competition, one can expect a reversed pattern of responsibility for proximity maintenance. Three measures were used to assess responsibility for proximity main- tenance: Hinde’s index of proximity: the proportion of ‘follows’ and ‘neighing’. The proportion of follows is the number of follows in relation to the number of departures within each dyad. Neighing is a vocalization emitted by males towards departing females. It is used as a measure of males’ motivation to negotiate proximity with females. The data come from focal observations on the silverbacks and ad libitum data collected over 8 months (380 h in 1989) at the Karisoke Research Center. Results indicate that within-group reproductive competition in itself does not lead to a reversed pattern of responsibility in proximity maintenance between males and females, but that the stability of the dominance relation- ship between the males, and the quality of the relationship between males and females, might have a role to play as well. Results on the neighing vocalization suggest that males are eager to negotiate proximity with cycling females rather than with lactating or pregnant females.

P. S I C O ~ ~ E , Departement d’Anthropologie, Universite de Montreal, C.P. 6128 Succ. A, Montreal, QUE, H 3 C 357, Canada.

Introduction

Male reproductive competition plays a major role in shaping the social structure of gorillas (Gorilla gorilla beringei) (WRANGHAM 1979,1987; HARCOURT 1981; STEWART & HARCOURT 1987; WATTS 1989, 1990b). Competition among males is expressed most clearly during inter-group encounters, during which females can transfer between groups (HARCOURT et al. 1976; HARCOURT, 1978b,

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48 PASCALE SICOlTE

1981; WRANGHAM, 1979; STEWART & HARCOURT 1987; YAMAGIWA 1983, 1987b; SICOTTE 1993). Males sometimes use herding to prevent female transfer (SICOTTE 1993). Hence, inter-group male reproductive competition is manifested not merely through displays and contact aggression with other males, but also through direct attempts to control the movements of the females between groups. The aim of this paper is the expansion of our knowledge of male reproductive competition by documenting the effect of within-group male reproductive competition on male-female relationships in groups comprised of two reproductive males.

Intense reproductive competition is usually limited within gorilla groups by the fact that young males leave their natal group upon reaching sexual maturity (HARCOURT et al. 1976; HARCOURT 1978b). The breeding system and social organization of gorillas thus tends to be based on a single male (HARCOURT 1981; HARCOURT et al. 1981 b; FOSSEY 1983; STEWART & HARCOURT 1987; YAMAGIWA 1987a, b; SICOTTE 1993). The only threat to a male’s exclusive access to his females arises during interactions with extra-group competitors because females may transfer to another group during these encounters.

However, nearly 40 % of all groups include two silverbacks (HARCOURT et al. 1981 a; WEBER & VEDDER 1983). These males are related in most cases (HARCOURT 1979a; HARCOURT & STEWART 198l), being either father and son or half-brothers. Maturing males may stay and breed in their natal group under certain conditions (depending on, for example, the quality of the relationship between the males, their relative ages and the number of breeding females in the group), although their access to fertile females is constrained by the presence of the dominant male (HARCOURT 1979a,b; HARCOURT & STEWART 1981; HARCOURT et al. 1981c; STEWART & HARCOURT 1987; WATTS 1990a, b, 1991 a; SICOTTE 1993).

Female gorillas never travel on their own. This is possibly due to the potential risk presented by predators (SCHALLER 1963; STEWART & HARCOURT 1987; DUNBAR 1988; WATTS 1990b) and most probably to the threat of infanticide by outsider males (WRANGHAM 1979, 1986, 1987; FOSSEY 1984; WATTS 1989,1990b). Females then seem to have obvious advantages in following a leader that can offer protection against these threats (WRANGHAM 1979, 1986; SMUTS & SMUTS 1994).

Theoretically speaking, in single-male groups and in the absence of a challenge from extra-group competitors, a male should not need to exert control over his females to keep them in his group. This should be reflected in the dynamics of the relationships between the sexes. SMUTS (1985) suggested that the individual most responsible for the maintenance of a relationship is the one benefiting most from this relationship. If this suggestion is valid, one expects females in single- male groups to be more active in promoting their relationship with the male than the male himself vis-h-vis the females, since females gain protection from their association with a male. Indeed, HARCOURT (1979b) showed that in single-male groups, females had a tendency to be more active in pursuing proximity with their leader, proximity being one important indicator of an affiliative relationship in gorillas.

In contrast, one can expect males in bi-male units to display greater responsi- bility in their relationships with females, because the presence of a second male

Male-Female Relationships in Mountain Gorillas 49

in the group induces within-group reproductive competition. A comparison of male behaviour in single- and bi-male units could show that males in bi-male groups are more responsible in their relationships with females than males that do not face within-group competition (TILFORD & NADLER 1978; WATTS 1992). This could be the case even if, overall, females still display greater responsibility in the relationships.

O n the other hand, it is also possible that the pattern between males and females in single and bi-male units, respectively, could be mutually opposing: bi- male groups could display a greater overall male responsibility in the maintenance of relationships with females, as opposed to a greater overall female responsibility in single-male groups. This latter suggestion was tested in this study. If a greater overall male responsibility is indeed observed in bi-male units, it could represent a method of male-control of female movement. This pattern of behaviour could be considered a functional within-group equivalent of the herding observed during inter-group encounters (SICOTTE 1993).

Some studies have reported that the presence of a second male in the unit does not alter the pattern of relationships between males and females (HARCOURT 1979b, 1981; HARCOURT & STEWART 1981; HARCOURT et al. 1981c), but these second males were adolescents. In a study done after a wave of immigration in a bi-male group, WATTS (1992) showed that neither resident females nor the old silverback were taking the primary responsibility for proximity, whereas newly immigrant females were active in seeking proximity with the young silverback.

This paper investigates the dynamics of male-female relationships in two bi- male units during a period of stability: no transfer had occurred among the groups for at least 1 yr and none took place during the study period. The relationship between the males was examined to establish to what extent their coexistence induces a competitive situation for access to the females. The maintenance of proximity in male-female dyads was analysed using three measures: Hinde’s index of responsibility for proximity; the proportions of follows in relation to the number of departures and the proportions of neighings, a vocalization emitted by males. It will be shown that this vocalization can be used as a measure of a male’s motivation to negotiate proximity with females.

Methods

Study Site and Subjects The data were collected during a 20-month field study conducted at the Karisoke Research Center

between Oct. 1987 and Oct. 1989. Groups in the study area (WATTS 1991 b) had been studied since 1967. Two reproductive groups were followed: Group 5 (n = 25) and Beetsme’s group (n = 12). Both units included LWO silverbacks (Table 1). In Group 5, Ziz and Pablo (18 and 15 yr old) were half- brothers through the paternal line. Beetsme and Titus (ca 25 and 15 yr old) were not related but have known each other since Beetsme (then a young blackback) transferred into Titus’ natal group. Beetsme is the only male known to have transferred into a reproductive unit (FOSSEY 1983).

Data Collection and Analysis The data presented here come from the last 8 months of the period of data collection (108 days).

50 PASCALE SICOlTE

Table 1: Adult composition of the two study groups

Groups SB Bb AdF SubF

Beetsme’s 2 0 3 4 Group 5 2 2 1 1 0

SB: silverback (over 12 yr); Bb: blackback (9-12 yr); AdF: adult female (over 8 yr); SubF: subadult female (6-8 yr)

The analysis is restricted to this period to ensure that the behaviour displayed, in particular the neighing vocalization, was properly identified. Focal observations were conducted on the four silverbacks, (Ziz: 108.5 h, Pablo: 23.1 h, Beetsme: 79.4 h, Titus: 48 h). Ad libitum observations on male-female and male-male relationships were collected in both groups (121 h). Ad libitum data also arose from the fact that a male was visible during focal observations on the other silverback.

Agonistic, affiliative and sexual interactions were recorded continuously. Aggression included low-intensity behaviour such as the ‘pig grunt’ (FOSSEY 1972; HARCOURT et al. 1993: ‘cough grunt’), the ‘cough grunt’ and other behaviour of increasing intensity such as charging and contact aggression. Avoidance was used to assess subordination, from simply moving aside from an approaching animal to crouching on the ground during an attack. Proximity (defined below) to the focal animal was taken every 5 min using instantaneous sampling (ALTMANN 1974). The activity of the majority of the group members (either feeding or resting) was recorded at the same time.

In the analyses of male-male aggression, focal observations from both males and ad libitum observations were combined. These observations are the equivalent of all occurrences of aggression between the males (ALTMANN 1974). In the analyses of male-female interactions, focal and ad libitum observations were combined because the data used for comparisons were always based on behaviour performed within a dyad (for example, the number of departures from an individual where he/she is being followed; see below).

Statistical testing methods were taken from SIEGEL & CASTELLAN (1988). All statistical tests were two-tailed. Results were considered significant if p < 0.05.

Effect of Activity Patterns on the Direction of Interactions

Activity patterns (feeding or resting) have been reported to influence the direction of interaction taking place between individuals and especially the time they spend in proximity (HARCOURT 1978a). Consequently, it has been suggested that the data from the rest period are ‘more relevant to a consideration of which partner was more responsible for the majority of their time in proximity’ (HARCOURT, 1978a, 1979b). In this study, only the direction of interactions was analyzed. The proportion of approaches and departures performed by the male within each male-female dyad was tested between feeding and resting periods to see whether the type of behaviour was affected by the pattern of activity. There was no significant difference (Wilcoxon matched-pairs signed-ranks test, Beetsme’s group; n = 20, z corrected for ties, = - 0.392, p = 0.7. Group 5; n = 25, z corrected for ties = - 1.198, p = 0.23). The data from feeding and resting periods were thus combined in all analyses.

Definitions

Reproductive State of Females. Adult and sub-adult females can be cycling, pregnant or lactating. Cycling and pregnant females are further divided into proceptive and non-proceptive females (pregnant females undergo post-conception estrus; STEWART 1977; HARCOURT et al. 1980, 1981 c; NADLER 1989; WATTS 1991 b). Nulliparous gorilla females display a slight sexual swelling, but estrus is deduced by behavioural clues in wild parous females because there are no obvious external indications of ovulation (HARCOURT et al. 1980).

Estrous Days. A day was referred to as an ‘estrous day’ when there was at least one proceptive female in the group. Some estrous days included two or more proceptive females (6 d out of 15 in Beetsme’s group and 10 out of 25 for Group 5).

Male-Female Relationships in Mountain Gorillas 51

Responsibility for Proximity between Males and Females. The behaviours used to assess responsi- bility for proximity are approaches and departures (a departure differs from a retreat in that it does not follow immediately on from an approach from the other member of the dyad). An approach or a departure was scored every time an individual increased or decreased the distance (5 m) to the other member of a particular dyad. An approach immediately followed by a departure from the same individual was categorized as ‘passing by’.

The proximity index (HINDE & ATKINSON 1970; HINDE & POWELL-PROCTOR 1977) was calculated for each male-female dyad by subtracting the proportion of departures made by the male, out of the total number of departures made by both members of the dyad, from the proportion of approaches that he performed out of the total number of approaches made by both members of the dyad. A positive index indicates that the male was more active in maintaining proximity with the female and a negative index that the female was more active. The index is not reliable for small frequencies (HINDE & POWELL-PROCTOR 1977; SMUTS 1985; HILL 1987, 1990). However, the minimum acceptable total of approaches and departures per dyad varies among studies. In the present study, dyads that displayed less than 14 approaches and departures were not included.

Interactions where an individual followed another who just departed were called ‘follows’. The number of follows in relation to the number of departures within each dyad was called the proportion of follows and was used as another measure of the responsibility for proximity maintenance. An individual had to leave the other member of the dyad at least three times for this value to be included in the sample.

Only the interactions where the recipient of a particular type of behaviour could be clearly identified were included in the sample. For instance, a female approaching a group of resting individuals was not recorded as approaching any of them in particular, not even the silverback, who is usually the focus of such groups, unless she engaged in some behaviour that allowed identification of the target of the approach (direction of the gaze or multiple approaches toward the same individual over a short period). The same was true for departures and follows that occurred at the end of the rest periods: it is typical for some males to leave the group and display at the end of the rest period (SCHALLER 1963), inducing the females to follow. Such events were not dyadic and their directionality could not always be assessed. As a result, they were not retained in the analysis of responsibility. Approaches directly linked to soliciting or mounting during a copulation, and departures following a copulatory mount were not retained either.

Neighing. The neighing vocalization (SCHALLER 1963; FOSSEY 1972: ‘whinny’) is emitted by male gorillas as part of male-female within-group interactions. Neighing is produced almost exclusively by silverbacks (a few have been heard from blackbacks). It is reminiscent of the neighing of a horse. The sound is a deep vibrato growl that starts with a high pitched sound and stabilizes at a lower pitch. I t lasts 2-3 s. This vocalisation is different from the ‘train grunt’, which is also a deep vibrato growl. However, the train grunt does not start with a high pitched sound and is linear in structure (HARCOURT et al. 1993). This last vocalization is used to solicit copulations ( W A ~ S 1991 b). It can be produced by both males and females, although males emit it more often.

This section examines the context of the occurrence of neighing and tries to establish its apparent significance. These analyses are presented here because they aim to show how this vocalization could be used as a behavioural unit in the study of the dynamics of male-female relationships in gorillas.

The most frequent context of emission of neighing seemed to be a female leaving the proximity of a male. When a female departed from a male, it was not unusual for her to do so in a sequence of movements. Each of these movements was apparently liable to provoke a neighing. For this reason, in all analyses concerning neighing, the term ‘departure’ includes every instance, separated by at least 1 min, of a female moving away from a male, either because she was near him and departed or because she was passing by him.

Neighings directed to each female by a silverback were classified as occurring after the female had departed from him or not (Beetsme’s group: n = 89; Group 5: n = 51 neighings in total; n towards individual females range from 3 to 43 with a mean of 8.4). This was done regardless of the female’s reproductive state. Males neighed significantly more when the females were leaving them than when no other behaviour was apparent (Fig. 1)

In order to rule out the hypothesis that males will emit any vocalization at all when faced with a departing female, one needs to compare the context of the occurrence of neighing with other close calls. The same analysis was thus performed using belches (FOSSEY 1972), also referred to as ‘syllabled

52 PASCALE SICOTTE

Beetsme’s group Group 5

Fig. 1: Proportion of neighings given to females (Wilcoxon test, Beetsme’s group: n = 1 1 , z corrected for ties = - 1.993, p = 0.046. Group 5: n = 14, z corrected for ties = - 2.7, p = 0.007)

doubles’ (HARCOURT et al. 1993). These are used in a variety of contexts, one of them being the negotiation of proximity between individuals, especially when a subordinate gorilla approaches a dominant one (HARCOURT et al. 1976, 1993). However, males can also emit doubles when a female leaves them. All doubles from a male following the approach or the departure of a female have been used for this analysis. (Beetsme’s group: n = 62; Group 5: n = 47 doubles in total; n towards individual females range from 0 to 1 9 with a mean value of 6.1). Note that while moving towards, or away from, a male, the female can also emit a double. A female departing from a male’s proximity was not the main context in which a male would emit a double. In Beetsme’s group, there was no significant difference between the two contexts (Wilcoxon test, n = 11, z corrected for ties = - 0.458, p = 0.647). In Group 5, doubles were directed significantly more often at an approaching female (Wilcoxon matched-pairs signed-ranks test, n = 17, z corrected for ties = - 2.813, p = 0.005).

It can therefore be reasonably argued that neighing is emitted towards departing females. After a male has neighed at a departing female, four possibilities can occur. Firstly, nothing more happens: The male does not move and the female continues her departing movement. Secondly, the male follows the departing female or thirdly, he follows her with his gaze (so as to monitor her and to know her location). Finally, the female interrupts her departing movement. If any of the last three possibilities occurred, proximity was said to have been successfully negotiated between the male and the female. Indeed, both members of the dyad were still in proximity or the male knew the location of the female, presumably in relation to the other male (in the cases where he ‘follows with the gaze’). Because neighing is emitted by males, it can be argued that males take the initiative in these negotiations and that the females then choose whether to stay or not.

Are males successful in their negotiation of proximity with females? That is, d o the last three possibilities occur more often than the first one? For this analysis, all females’ departures from a male were used (Beetsme’s group: n = 57 departures with neighing and n = 239 departures without neighing; Group 5: n = 29 departures with neighing and n = 159 departures without neighing).

In the first analysis, only departures with neighing were considered. The proportion of cases where males were successful in preventing departure was compared to the proportion of cases where they were not. The results showed no significant differences (Fig. 2a)

In the second analysis all the females’ departures from a male were used. The proportions of departures where proximity was successfully negotiated were compared, depending on the presence or absence of neighing. The proportions of departures where proximity was successfully negotiated after neighing tended to be larger in both groups, and the tendency was significant when the groups were combined (Fig. 2 b)

However, the same analysis needs to be conducted with doubles to rule out the possibility that proximity could be successfully negotiated using any vocalization at all. The emission of a double by

fS

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9‘0

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54 PASCALE SICOITE

Tuble 2: Antagonistic interactions between silverbacks in the two study groups ~~

Antagonistic Aggressor episodes Ziz Pablo Beetsme Titus

~~~~~~~~~ ~

Uni-directional 74 (7)' 10 82 (7)' 37 (2)' aggression I aggression

Bi-directional 6 1 7 15

'number of times the aggression induced submission

Beetsme's group Oroup 5

Fig. 3: Direction of male-male aggression in relation to the presence of an estrous female in the group (Mann-Whitney test: Beetsme's group: n, = 9, n2 = 17, z corrected for ties = - 3.07, p = 0.002; Group 5: n, = 17, n, = 23, z corrected for ties = - 2.13, p = 0.034; only days where aggression occurred

were retained in this analysis).

significant (1.23 and 0.53; Mann-Whitney test, n, = 15, n2 = 29, z corrected for ties = - 1.095, p = 0.28).

In Group 5, aggression was sometimes bi-directional, although most aggressions flowed from Ziz to Pablo. Submission, however, was uni-directional: Ziz never submitted to Pablo (Table 2). The rate of aggression was 0.81 timeslh. No significant difference was found in the rate of aggression between estrous and anestrous days (0.85 and 0.79/h; Mann-Whitney test, n, = 25, n2 = 41, z corrected for ties = - 0.548, p = 0.58).

The presence or absence of high intensity aggression (charge or contact aggression) among males was also compared between the two categories of days (estrous and non-estrous). No significant difference was found in either group (Beetsme's group: X2 with continuity correction = 0.035, df = 1, p = 0.85. Group 5: Fisher test, n = 66, p = 0.59).

Finally, aggression directed to the dominant male might occur more often on estrous days. This was indeed the case (Fig. 3)

Male-Female Relationships in Mountain Gorillas

Non procrptive

Pr0ceptlv.

55

A. Illnde’s Index B. SB follows P

0 8

0 7

0 6

m OJ

0 4

0 1

T

Both groups Bcetsme’s grwp

C. Proportlon of nelghlngs

Both groups

Fig. 4: Effect of proceptivity on the responsibility of males and females in the maintenance of proximity: a. Wilcoxon test, Beetsme’s group: n = 3, z corrected for ties = - 1.60, p = 0.11 ; Group 5: n = 2, z corrected for ties = - 1.34, p = 0.045; both groups: n = 5, z corrected for ties = - 2.023, p = 0.04. b. Wilcoxon test, n = 5, z corrected for ties = - 0.944, p = 0.35. c. Wilcoxon test, Beetsme’s group: n = 6, z corrected for ties = - 0.734, p = 0.46; Group 5: n = 3, z corrected for ties = 1.069,

p = 0.28. Both groups: n = 9, z corrected for ties = 0.59, p = 0.96

Male-Female Relationships: Responsibility in Proximity Maintenance

Both males will, if possible, attempt to maintain affiliative relationships with the females and this should be reflected in their attempts to maintain proximity. In fact, within each group, males did not differ in their values for the three measures of the maintenance of proximity, although there was a tendency for females to follow Beetsme more than Titus (Mann-Whitney test, 1 . Hinde’s index: Beetsme’s group: n, = 5, n2 = 6, z corrected for ties = - 1.461, p = 0.14; Group 5: n, = 1 , n2 = 14, z corrected for ties = - 0.579, p = 0.56. 2. Proportion of follows, silverback follows female: Beetsme’s group: n, = 6, n2 = 8, z corrected for ties = - 0.464, p = 0.65; Group 5: n, = 1 , n2 = 12, z corrected for ties = 0, p = 1 , female follows silverback: Beetsme’s group: n, = 2, nz = 4, z corrected for ties = - 1.853, p = 0.064; Group 5: Pablo had no value. 3. Proportion of neighing: Beetsme’s group: n, = 9, n2 = 9, z corrected for ties = - 0.929, p = 0.35; Group 5: nl = 7, n2 = 15, z corrected for ties = - 0.887, p = 0.37). Males in each group were combined for the following analyses.

Effect of Proceptivity Males tended to be more active than females in the maintenance of proximity

when the females were proceptive than when they were not, in Beetsme’s group. This tendency is significant in Group 5 and when the groups are combined (Fig. 4 a)

56 PASCALE SICOTTE

0 L.C+.ll.,

PI.,...‘

Cycling A

0.4-

Both groups X

Fig. 5 ; Effect of the reproductive state of females on the responsibility of males in proximity maintenance with females (Hinde’s index). Kruskal-Wallis test: n = 3, df = 2; Beetsme’s group: H corrected for ties = 4.33, p < 0.2; Group 5: H corrected for ties = 2.45, p < 0.2; both groups: H

corrected for ties = 4.62, p < 0.1

The effect of proceptivity on follows was tested by comparing the proportion of follows made by males towards proceptive and non-proceptive females. This could be done for Beetsme’s group only. No statistical difference emerged (Fig 4b) The proportions of follows made by males towards proceptive females could also be compared to the proportion of follows by the females themselves. In Beetsme’s group, there were 5 dyads with sufficient data on male follows, but only one dyad with the minimum number of male departures required to calculate the proportion of female follows. This suggests that although males did approach proceptive females in Beetsme’s group, they did not often leave them.

Proceptivity did not significantly influence the proportion of neighings received by the females (Fig. 4c)

Non-Proceptive Females: Effect of Reproductive State Males facing within-group reproductive competition should prefer to maintain

proximity with cycling females as opposed to lactating or pregnant females. Using Hinde’s index, males did not appear to be more active than females in pursuing proximity with cycling females (Fig. 5).

HARCOURT (1979 b) showed that in single-male groups, females followed silverbacks more often than vice-versa. The same was true in this study for Group 5 but not for Beetsme’s group (Fig. 6 ) . This strengthens the previous results on the effect of proceptivity : males from Beetsme’s group followed their females more than males in Group 5 .

The reproductive state of females did not seem to influence the proportion of their follows (Fig. 7) nor did it seem to influence the proportion of follows made by males (Fig. 8).

LS

58 PASCALE SICO~TE

Btttsme's group Group 5

Fig. 8: Effect of reproductive state of females on male follows (Kruskal-Wallis test: n = 3, df = 2; Beetsme's group: H corrected for ties = 0.11, p < 0.9; Group 5: H corrected for ties = 2.397, p < 0.5)

-3 0.7

0.6 d

a Od/ T

Beetme's group * Both Oroups

+ Group 5

Fig. 9: Effect of the reproductive state of females on the proportion of neighings. "significant difference. (Kruskal-Wallis test: n = 3, df = 2; Beetsme's group: H corrected for ties = 3.572, p < 0.2; Group 5: H corrected for ties = 10.885, p < 0.01, both groups: H corrected for ties = 15.485,

p < 0.001)

Discussion

Male reproductive competition is important in shaping the gorilla social system and is most apparent during inter-group encounters (HARCOURT et al. 1976; HARCOURT 1978b, 1981; WRANGHAM 1979, 1987; STEWART & HARCOURT 1987; YAMAGIWA 1987b; WA'ITS 1989, 1990b; SICOTTE 1993). Little is known, however, about the relationship between coexisting males or the impact of within- group male competition on male-female relationships. The functional aspects of male coexistence are not well understood either. Bi-male units might have an advantage in inter-group encounters (FOSSEY 1983; WRANGHAM 1986; STEWART & HARCOURT 1987; WATTS 1989; SICOTTE 1993), but it is not always clear why

Male-Female Relationships in Mountain Gorillas 59

silverbacks should tolerate a rival, especially when the majority of the groups include only one male.

The results presented here on male aggression showed that dominant males are aggressive towards young silverbacks, who sometimes retaliate, especially on estrous days. This suggests that the presence of a younger male might not be due simply to the greater tolerance of the dominant silverback. A better description would be that despite the fact that they receive aggression, young males sometimes resist eviction. The intensity of this resistance might be linked to the number of breeding females in the group, to the relative age of the males and to their relatedness (HARCOURT et al. 1976; HARCOURT 1979a; YAMAGIWA 1987b; WATTS 1989; SICOTTE 1993). The older male’s tolerance might be linked to the benefits that he derives from the presence of the younger male during inter-group encounters, particularly when the other groups in the area are also bi-male.

The fact that aggression from the subordinate male towards the dominant male was more frequent during estrous days in both groups, suggests that males compete over access to the females (BERENSTAIN & WADE 1983). The presence of proceptive females in the group did not affect other aspects of male relationships such as the intensity of, or overall rate of, aggression. This is consistent with previous findings showing that within-group competition among males is relatively mild compared with competition between groups (HARCOURT 1981 ; HARCOURT et al. 1980, 1981c; YAMAGIWA 1987b), a pattern also shown by chimpanzees (TUTIN & MCGINNIS 1981; HARCOURT et al. 1980; GOODALL 1986; but see DE WAAL 1986).

Responsibility of Males and Females in Proximity Maintenance Proximity between individuals of opposite sexes in primates can be maintained

by means of aggressive behaviour- such as herding or mate guarding- used by the male. This is especially true when the female is in estrus. Affiliative behaviour, grooming for example, can also have the same effect (BERENSTAIN & WADE 1983; SMUTS & SMUTS 1994). This study focused on other behaviour that relates to proximity maintenance in gorillas: approaches and departures, follows and neigh- ing. The underlying assumption is that the sex that is most responsible for proximity maintenance is the sex that gains more from the relationship (SMUTS 1985).

In this study, males were more responsible for maintaining proximity with proceptive than with non proceptive females, as measured by Hinde’s index. Also, it has been impossible to compare the proportions of follows made by the silverbacks to those made by proceptive females in Beetsme’s group, because males rarely left proceptive females. Males would sometimes literally follow the females step by step as they were moving away from them. There are no comparable data differentiating estrous and anestrous females for proximity maintenance in single- male groups. Females have been shown to spend more time in proximity to the leading male when in estrus (HARCOURT 1979a) but whether this results from the

60 PASCALE SICOTTE

male seeking access to the female or from the female approaching the male is unknown.

Proceptive females did not receive more neighings than non-proceptive females, however. This may indicate that the males did not need to neigh towards proceptive females to negotiate proximity because they were already responsible for maintaining proximity with them.

Gorillas do not establish consort relationships (HARCOURT et al. 1980), but if maintenance of proximity during estrus is considered equivalent to the maintenance of a consortship, these results from bi-male units are consistent with observations from other primates living in multi-male groups, where males show more initiative than females in the maintenance of consortships (BISHOP 1979; BERENSTAIN & WADE 1983; GOODALL 1986; SMUTS & SMUTS 1994).

Among non-proceptive females, neither males nor females appeared to have a greater responsibility in maintaining proximity according to Hinde’s index. In Group 5, females followed males more than vice-versa. This is similar to the tendency found in single-male groups (HARCOURT 1979b). This was not the case in Beetsme’s group, however, where these two proportions showed no statistical difference. Furthermore, the comparison of the follows made by the males towards proceptive and non-proceptive females in Beetsme’s group showed no statistical difference, indicating that these males were as eager to follow proceptive as non- proceptive females.

These results generally indicate that within-group male reproductive competition does not simply lead to the inversion of the pattern of respon- sibility suggested in the introduction. One could test the alternative hypothesis that males in bi-male units are more responsible than males in uni-male groups, but this increase in responsibility would not be sufficient to lead to a reversal of the pattern.

The males in Beetsme’s group, however, showed more initiative in the maintenance of proximity than those in Group 5. It is noteworthy that at the time the dominance relationship between Beetsme and Titus was unstable, leading to more overt competition. A reversal of the pattern of proximity maintenance between males and females could not then be simply the result of within-group reproductive competition, but could possibly be the result of an unstable dominance relationship between the males. When priority of access in relation to dominance is unstable, males may switch to an alternative strategy to gain access to females. Furthermore, whether the group is newly formed or well-established (HARCOURT 1978 b; SICO~TE 1993) perhaps influences the way males and females maintain their relationship. For example, WAITS (1992) worked on Group 5 after a wave of immigration. In his study, neither the males nor the females took the primary responsibility in the relationships between the resident females and the old silverback, whereas new immigrants were active in seeking proximity with the young male. WATTS (1991a, 1992) reported that the group was occasionally splitting during the study: the old male and the resident females would form a subgroup while the young silverback and the immigrants would form another one. The dynamics of male-female dyads within each subgroup were perhaps

Male-Female Relationships in Mountain Gorillas 61

different when the two subgroups were joined: it could have resembled two single- male groups, a first, well-established group and a second, newly formed. Also, the resident females frequently harassed the immigrants. This might have induced the immigrants to seek proximity to the young silverback, who regularly intervened on their behalf (WATTS 1991 a). In the study presented here, Beetsme’s group was relatively new compared to Group 5.

Finally, cycling females received a larger proportion of neighings than lactating females. This suggests that males were eager to negotiate proximity with females that were likely to be mating partners, or with potential migrants (SICOITE 1993). The fact that the negotiation of proximity was not always successful from the male’s point of view is probably an expression of female choice. It would be interesting to test whether a female that does not respond to neighing is more likely to either transfer to another group or to mate with the second male in the group.

The Neighing Vocalization

Neighing by a silverback towards a departing female could be a way to negotiate proximity. The fact that it was not always successful should not invalidate this vocalization in the analysis of social relationships. Social interactions are always the result of a compromise between the motivations of both members of a dyad.

In this study, sample sizes were too small to discriminate male and female responsibility in the maintenance of proximity after a neigh. However, it will be important in future research to determine the proportion of cases where females stop their departing movement upon hearing the neighing as opposed to cases where males follow the females. The context of emission of the neighing vocal- ization identified in this study was a female leaving a male. This is probably not the only context in which this vocalization is emitted, however. It was simply not apparent from the available data that there was another situation where neighings were given that could be identified. In some cases, a male neighed at a female sitting close by; perhaps subtle clues had indicated that the female was about to leave.

The neighing is possibly expressed in the context of within-group male reproductive competition. In order to verify this hypothesis, one would need to show that males in single-male groups do not neigh towards their females. If this is the case, it would explain why the neighing was not often reported and why it was not used before in the analysis of social interactions in gorillas. Indeed, a good proportion of the published data available on mountain gorillas come from studies in single-male groups. A further argument for this interpretation comes from FOSSEY’S observations (1972). She reported this vocalisation after having heard it from only one male. She seemed inclined to classify it as idiosyncratic because he was old and sick. However, this group also included a young silverback (FOSSEY 1983; WATTS, unpubl. data). The possibility remains, however, that the neighing vocalization is regularly emitted in both single and bi-male units, but

62 PASCALE SICOTTE

that it has been categorized with other close calls emitted by gorillas (HARCOURT et al. 1993).

Acknowledgements

The author thanks I’Office Rwandais du Tourisme et des Parcs Nationaux (Rwanda) and I’Office Zairois pour la Conservation de la Nature (Zaire) for permission to work in the Parc National des Volcans and in the Parc des Virunga. I also thank The Dian FOSSEY Gorilla Fund for permission to work at the Karisoke Research Center. My fieldwork has only been possible with the help of the staff at Karisoke. M. LECOMTE, J. MILNER, S . TEIJEIRO, P. VASEY, Drs J. PRUD’HOMME, B. CHAPAIS, D. P. WAITS and an anonymous reviewer made valuable comments on earlier versions of the manuscript. I am indebted to Dr B. CHAPAIS for his support. This work was supported by the Natural Sciences and Engineering Research Council of Canada, the Fonds pour la Formation de Chercheurs et 1’Aide a la Recherche of Quebec, the Universitk de Montreal, the L. S. B. LEAKEY Foundation and The Dian FOSSEY Gorilla Fund. This is publication no. 129 of the Karisoke Research Center.

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Received: January 21, 1993

Accepted: January 7, 1994 (J. Brockmann)