Keywords

1 Mountain Gorilla Social Systems

Mountain gorillas (Gorilla beringei beringei ) are characterized as living in stable, cohesive, polygynous groups typically composed of one adult male “silverback” and a median of five adult females, together with their offspring (Harcourt and Stewart 2007). Silverback is the term used for mature male gorillas from the age of 12 years, when hairs on the saddle of the back start to turn grey, and some individuals are already capable of siring an infant at that age (Bradley et al. 2005). Silverbacks are considered to be fully grown by age 15 (Watts 1991; Watts and Pusey 1993), by which time 50 % of them are likely to have left their natal group and become solitary (Robbins 1995; Watts 2000). The other half of the silverback population does not leave the natal group, and thus groups can become multimale (Watts 2000; Robbins 2001, 2003). Although gorillas are considered to have evolved in a one-male mating system, a significant proportion of mountain gorilla groups contain two or more silverbacks. In their age-graded social system, a hierarchy exists amongst the adult male gorillas, and competition among the males can be intense, particularly when females are in estrus (Harcourt et al. 1980; Robbins 2003). Males that had a strong affiliative relationship with a dominant silverback when they were infants are more likely to remain in their natal group (Harcourt and Stewart 1981), and a few eventually inherit leadership of that group. The accepted model of new group formation is that females transfer out of a group to join a solitary male, or that a breeding group splits permanently into two units.

Nearly 500 mountain gorillas live in the 455-km2 Virunga Volcanoes of the Democratic Republic of Congo, Rwanda, and Uganda (Gray et al. 2013). The groups studied by the Karisoke Research Centre , in Rwanda, have been habituated to the presence of human observers and can be individually identified. In just one generation, these groups have shown striking increases in both size and the number of adult males per group, with few males emigrating. At the beginning of this study, in January 1996, the research population comprised 73 gorillas in three groups of 19, 23, and 31 individuals, each with one or two adult male silverbacks. Six years later, the population had grown to 98 gorillas with 24, 27, and 47 individuals in the same three groups, and three to six adult males per group (Williamson and Gerald–Steklis 2001) (Table 14.1). I describe changes in the structure of the Karisoke population, consider how they have occurred, and present some implications for the management of this Critically Endangered primate.

Table 14.1 Composition of three Karisoke mountain gorilla groups at beginning and end of this study
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2 The Karisoke Mountain Gorilla Population 1996–2001

The 1994 genocide in Rwanda brought a halt to intensive behavioral research on the Karisoke mountain gorillas. During the periods of insecurity and military conflict that followed, great efforts went into monitoring the gorillas and maintaining demographic records, while behavioral data were collected within the constraints of limited access to the gorillas. During this study, researchers were unable to enter the Volcanoes National Park from June 1997 to September 1998 (the park remained closed to tourists until July 1999). Observations were interrupted again between May and August 2001. Despite these difficulties, we consider the demographic records of these groups to be complete, as records of all births, deaths, and transfers have been maintained since 1967. The only demographic events that might have been missed would have been infants that were born during the 16 months when we had no access to the gorillas but which did not survive.

During this study, ten young male gorillas in three research groups matured into silverbacks. Based on our prior knowledge of gorilla demography, we expected four or five of these males to emigrate, but only one left his group to become solitary (at age 13.2 years). One died (aged 14.9 years) following infection of bite wounds inflicted during an aggressive encounter with another gorilla group, and three attained full physical maturity (i.e., reached 15 years of age) in their natal groups (Table 14.2).

Table 14.2 Ages of adult male mountain gorillas in this study
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This low rate of emigration (10 % in this study compared to 36 % in the preceding three decades; Robbins 2001) was not a consequence of subordinate males being permitted to stay with impunity, as they were subject to aggressive attacks by the dominant male. Behavioral observations were conducted on two of the three Karisoke research groups, one of which (the SHI group) included three to six silverbacks, whereas the other (the PAB group) was unusually large (31–47 individuals during this study), with three silverbacks. Hierarchies among the males were determined using pair-wise displacements recorded between July 1999 and June 2001 (cf. Robbins 1996), a period when access to the park was consistent and data collection was regular. Rank correlated with age for all but two males: the oldest, a post-prime silverback in PAB group, and a young silverback in SHI group who was physically inferior to the rest of his cohort (undersized with a sway back).

3 Intragroup Aggression

Analyses of aggression focused on the young competitors over the same 2-year period, excluding a former dominant male (PAB) who had been deposed but not evicted from the group and no longer posed a challenge for leadership. Two levels of physical aggression were distinguished: (1) medium—when a single bite was observed, or one or two wounds recorded (e.g., Fig. 14.1), and (2) severe—when biting was repeated, or visible wounding was extensive. Attacks by the dominant males (CAN and SHI) were almost always directed at one particular individual in their group (UMR in PAB group and NTA in SHI group; NTA was the highest ranking and most physically developed of five young silverbacks). The level of visible wounding of these two silverbacks was not observed with other individuals, and attacks intensified when they reached the ages of 13.5 years (UMR) and 12.4 (NTA), respectively. Attacks classed as “severe” lasted up to 3 min and often resulted in serious wounding. Gashes 6–15 cm long were seen on top of the head, side of face, back of neck, shoulder, back, inner arm, and hands. During attacks, both protagonists were generally silent, although onlooking females screamed. Victims were often pinned down and did not retaliate or defend themselves. They filled the air with a characteristic pungent male odor (silverbacks emit a musky odor from axillary glands in the armpit in situations of fear or excitement) and sometimes passed diarrheic dung during or immediately after the attack. Adult females occasionally tried to intervene during the dominant silverback’s attacks, as did the former dominant male in PAB group on one occasion. In SHI group, the victim’s mother once attempted to bite the attacking dominant silverback, but on two occasions other group members joined in the assault.

Fig. 14.1
figure 1

Subordinate silverback mountain gorilla with a bloody nose after being attacked by the dominant silverback. (© DFGFI)

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Intragroup aggression was scored from bite wounds, even if an attack had not been observed, but only when no intergroup interaction had been recorded in the preceding days. Watts (1996) noted that silverbacks receive progressively more aggression from older males as they mature, and severe aggression was recorded during 16 of the last 20 months of this study. SHI made 80 % of these attacks on NTA, despite the presence of four other young silverbacks maturing in the cohort. As the other males aged, SHI’s attacks were also directed at the fourth ranking (from the age of 13.5 years) and fifth ranking (from age 13.2 years); however, his aggression toward NTA did not diminish. Interestingly, the third-ranking male (UGE) was the only silverback in the cohort observed to display any affiliative behavior with the dominant male, and he was rarely attacked.

Most attacks seemed to occur without provocation other than proximity. We might expect aggression to increase at times when competition for females was highest, that is, when females were in estrus and would typically copulate repeatedly over a 3- to 4-day period (Czekala and Sicotte 2000). Using dates of parturition, I estimated the number of females in each group that could have been cycling each month during the 2 years. On average, 2 females per group were potentially cycling for a few days each month, although in the large PAB group with 17 adult females, it is possible that 8 females were cycling during the second quarter of 1999. No significant correlation was detected between the presence of cycling females and levels of aggression recorded; however, Watts and Pusey (1993) noted that rates of male–male aggression were influenced not only by the presence and number but also the identity of estrous females. Thus, the proxy used in this study may have been too simplistic.

Despite enduring frequent and severe attacks by the dominant silverback, some maturing males stayed with their group rather than becoming solitary. Thus, there was an obvious cost to remaining in their natal groups, and the question arises: why would these males tolerate such aggression?

4 Mating Opportunities and Companionship

Mountain gorilla females reach sexual maturity at about 8 years old and generally have their first infant between the ages of 9 and 10 years. While infants are suckling, their mothers experience lactational anestrus and are unable to conceive again for 3–4 years after giving birth. Therefore, opportunities to mate are rare, even though females may copulate with more than one male (Robbins 2003), and a male’s emigration decisions will be influenced by the number of adult females and the number and age of male competitors in his group (Robbins 1995; Watts 2000).

Dominant males do not readily tolerate copulations by subordinate males, and harassment by the dominant of another male or toward the female is well documented (Robbins 1999). Although dominant males participate in the majority of copulations, in this study nine of the ten subordinate silverbacks were seen to copulate at least once with an adult female. On one occasion when NTA was copulating, the dominant male ran at and bit him severely. However, almost all observed copulations by subordinates were surreptitious—copulatory vocalizations were subdued or suppressed—and did not attract the attention of the dominant silverback (n = 32). Genetic studies have since revealed that subordinate silverbacks occasionally sire offspring (Bradley et al. 2005).

The high ratio of 5.6 adult females per adult male in PAB group reveals a factor likely to have had a strong influence on the three silverbacks remaining together; however, this would not explain the situation in SHI group with six resident males and only 1.2 females per male. Reproductive competition is a key determinant of reproductive strategy, but in this highly gregarious species another factor must also play a role: life in the company of others. Subordinate silverbacks who stay in their natal group have at least an occasional opportunity to mate; they also continue to engage in social interactions such as grooming. To support this hypothesis, we can cite the former existence of two all-male groups at Karisoke: male gorillas that chose to live in a group environment where individuals could interact with one another and further their social skills, but which clearly did not contribute to their reproductive success (Yamagiwa 1987a; Robbins 1996; see also Stoinski et al. 2001, 2004).

5 Risk of Injury

Attempting to obtain females from another silverback is a high-risk venture, which can lead to physical injury and even death; thus, opting for a solitary strategy is also costly. During this study, three adult male gorillas were fatally wounded: we found the bodies of two lone silverbacks with trauma to the head and genitalia, consistent with injury inflicted during confrontation with another silverback. The third fatality was a group-living subordinate silverback who died of septicemia following an injury sustained during an intergroup encounter.

If the chances of acquiring a female were high enough, the risks involved in pursuing a group might be worth incurring, but it seems they are not. During the first 35 years of study of the Karisoke mountain gorillas, few solitary males succeeded in forming a new group or taking over an established group (Watts 1989, 2000; Robbins 1995, 1996, 2001; Harcourt and Stewart 2007). Group takeovers by a solitary silverback can occur when the dominant male in a one-male group dies or is killed, but these events have been rare. We can find examples of group takeovers among the other gorilla subspecies (Tutin 1996; Yamagiwa and Kahekwa 2001); however, in mountain gorillas, group acquisition has not occurred as a natural phenomenon, but as a consequence of poachers killing the dominant silverback.

During the present study, only one of the ten maturing silverbacks (INZ) became solitary. We observed several subsequent interactions between this individual and his natal group, and each time he was chased away by the subordinate males, his former playmates. Although in his prime and in excellent physical condition, he remained alone throughout (and beyond) this study. A significant disadvantage for this solitary male was that his home range overlapped with multimale but no one-male groups, and he would have had to lure females away from two or more silverbacks.

6 Multimale Groups

Most female mountain gorillas transfer from one group to another at least once during their lifetime (Watts 1996), and transfers usually take place during encounters between groups. Gorilla groups often exchange chestbeats and vocalizations from a distance, but when encounters escalate to aggression, fighting between adult males can be intense (Harcourt 1981; Watts 1991). Intergroup interactions are contests for access to adult females and occur about once per month in the Karisoke population (Sicotte 1993, 2001). Multimale groups are better able to retain their females because two or more silverbacks can cooperate during such encounters. Typically, one silverback herds females away from the frontline, which is effective in preventing female transfer, while the other rebuffs challengers (Sicotte 1993). Therefore, so long as the dominant male loses few matings or gains compensating payoffs in inclusive fitness, he may benefit by tolerating a younger silverback as an ally against extra-group males (Watts 1996). Subordinate males in the present study were indeed seen to play active roles in intergroup interactions.

The incidence of multimale groups in the wider mountain gorilla population (groups habituated for research and tourism) has increased from 40 % in 1981 to 61 % in 2010 (Gray et al. 2013). What is more extraordinary is that there are not just two but many silverbacks in some groups; each of the three research groups has included six or more silverbacks at some point in time. It is also notable that during this study, the rate of female transfer was low, both into (n = 2) and out of (n = 2) the research population, and between the three research groups (n = 5) (total number of adult females = 26–31).

Robbins (2001) noted that multimale groups perpetuate multimale groups, and a likely mechanism for this was elucidated by Parnell (2002): “If the presence of more than one silverback confers an advantage when acquiring new females or defending residents, a virtual ‘arms-race’ can be envisioned in which increasing numbers of silverbacks are required for a group to remain competitive. The dominant male may thus become more tolerant of subordinate males within his group. Ever greater numbers of adult males per group can be predicted with an inevitable decrease in numbers of solitary males, both as young males are tolerated in their natal group, and as the solitary route to group acquisition becomes increasingly unrewarding and potentially hazardous. Such a mechanism for the increase in multimale groups will have a ‘feedback’ effect on other groups. A group silverback unable to rely on coalition support may be more likely to lose females and encounter more difficulty in acquiring them. Creating conditions such that maturing males delay their emigration will be a powerful strategy for maintaining viable groups”.

Males that do not emigrate contribute to groups becoming larger not simply by their own presence but also because mountain gorilla groups with more than one male tend to attract and retain more females (Robbins 1995; Yamagiwa et al. 2009). Adult females associate with adult males as a means to avoid infanticide by extra-group males (Watts 1989). Infanticide is a reproductive tactic that shortens the time which elapses before lactating females become fertile again and has accounted for 26 % of infant deaths in the Karisoke population (Robbins and Robbins 2004). Apparently females favor groups with more than one adult male because they provide better protection against infanticide in the event of the death of the dominant male (Watts 2000; Robbins 2003). Interestingly, there were no cases of infanticide by adult males in the research groups during this study. This absence of infanticide was likely a consequence of the social stability of these groups, which would be consistent with Robbins’ (1995) prediction that infants in multimale groups should suffer fewer infanticidal attacks. [Two infant deaths occurred in 1996, but these were attributed to competition between new mothers and pregnant nulliparous females over the newborns, not deliberate killing by a potential mate (Warren and Williamson 2004)].

Sicotte (1993) observed that groups with more than two adult males did not exist in the Karisoke population and questioned why multimale groups were not more common at that time. However, as the research groups have grown in size and the number of resident females has increased, the likelihood of a number of male offspring growing up as a cohort has also increased, and this was the case in 1986–1987, when six male infants were born into Group 5 (the precursor to the PAB and SHI groups). By the end of the present study, the 25-year-old leader of SHI group was accompanied by five young silverbacks, 14–16 years old, and at least three of them shared the same father (Bradley et al. 2005). Watts (2000) suggested that closely related males (father and son or half-brothers) are likely to be more tolerant of one another than unrelated males, and this seems to be true of the SHI group silverbacks.

7 Social Stability and a Supergroup

The factors discussed above have combined to produce larger groups. Consider that in 1972 there were 96 gorillas in the Karisoke sector living in eight groups (Fossey 1983) and that in 2001 the same number could be found in just three groups. Group 5 grew in size to 35 members, five times the norm, before fissioning in 1993. The catalyst for this split was the death of the dominant male. We therefore expected the PAB group to fission when it surpassed 35 members; however, there was no catastrophic event to perturb the social balance and this group continued to grow, peaking at 65 individuals in 2006 (Vecellio 2008).

Various factors contribute to the formation and maintenance of large, multimale groups, and these have been discussed at length (e.g. Watts 1989, 2000; Robbins 1995, 2001, 2003; Robbins and Robbins 2005). Typically, a group will disintegrate when the dominant male of a single-male group dies, but when this happens in a multimale setting one of the subordinate males can take over leadership and the group remains intact, enabling offspring to mature in a stable social setting (Yamagiwa 1987b; Robbins 1995). Thus, group stability is largely assured by a multimale structure, and males who remain in breeding groups seem to have substantially higher fitness payoffs than males who emigrate. The principal advantages gained by residents are increased opportunities to mate and enhanced infant survival. It seems that solitary silverbacks have little chance of establishing a new group and reproducing successfully in this “arms race”.

So, are these changes typical of the population as a whole? Surveys of the Virunga population show that the median size of gorilla groups has not changed over 30 years (median 7.5, n = 32), but that mean group size has increased from 7.9 to 11.4 individuals, reflecting an increasing proportion of large groups (Gray et al. 2009). Habituated groups, and the Karisoke groups in particular, are significantly larger than unhabituated groups (mean, 16.8 vs. 5.9). The above-average size of gorilla groups in the Karisoke sector has been attributed to two principal factors: first, that habitat quality in this sector is better than in other sectors of the Virunga Volcanoes (McNeilage 2001), and second, the much higher level of protection afforded to the Karisoke groups through daily monitoring by gorilla trackers and researchers, which not only deters poachers but also facilitates rapid intervention by a veterinary team when needed (Kalpers et al. 2003).

8 Active Conservation and Management Issues

Since 1902, when mountain gorillas were first brought to international attention, human impacts on the Virunga population have been devastating, from their slaughter by museum collectors and trophy hunters to the clearing of more than half of their entire habitat in Rwanda in the late 1960s (Plumptre and Williamson 2001). Compounding the loss of habitat, targeted killing by poachers in the 1970s and early 1980s had a major impact on the gorillas’ demography, leading to group breakups or takeovers and further losses through subsequent infanticide (Fossey 1983). However, by the end of the 1980s the conservation status of the Virunga gorillas had improved dramatically, brought about by daily monitoring of the habituated groups and the expansion of antipoaching patrols.

The Virunga gorillas’ survival was again threatened throughout the 1990s, this time by civil conflict. Less well known than the 1994 genocide is that during 1997 and 1998 civilians fleeing armed conflict in Rwanda took refuge in the forests of the Virunga Volcanoes, building shelters and cultivating crops in the park, while armed militia controlled access to the region. Remarkably, these events left the Karisoke gorillas visibly unscathed. Active conservation has allowed the Virunga gorilla population to recover from an estimated all-time low of 254 and to attain 480 individuals in just 30 years, one and a half generations. Groups that are well protected do not suffer the same degree of human-induced mortality and habitat degradation that nonhabituated groups do and, with veterinary intervention, habituated gorillas no longer die of snare injuries. This is not the case for the entire population, and the unhabituated subpopulation is in decline (minus 0.7 % annual growth rate; Robbins et al. 2011). Consequently, mountain gorillas continue to be classified as Critically Endangered on the IUCN Red List of Threatened Species (Robbins and Williamson 2008), meaning that they face a high risk of extinction.

With a return to peace and stability in some sectors of the Virunga Volcanoes, military escorts have become a necessary accompaniment to research and tourism activities. The increased number of people in the park—tourists, trackers, researchers, and soldiers—is likely to have affected the gorillas’ demographic dynamics. Unhabituated groups rarely approach monitored groups and usually flee if human observers are present. Even if interactions between habituated and unhabituated gorillas still take place, they are infrequent and thus normal social dynamics may be impeded. Incest has perhaps become inevitable and is known to have occurred in one Karisoke group, in which the dominant silverback fathered an infant with one of his sisters and mated with at least one of his aunts. The mother and four other close relatives of this male were among the 17 reproductive females in his group. Many individuals in the research groups are closely related (Bradley et al. 2005), and inbreeding is manifested by strabismus and syndactyly (e.g. Routh and Sleeman 1997). Fewer transfers between groups would reduce gene flow and may increase the level of inbreeding. If the close and sustained presence of human observers is potentially compromising normal social interactions, behavioral disturbance must be minimized by observance of strict limits to the numbers of people tracking, the distance to which they approach gorillas (no closer than 7 m), and the duration of visits (see Macfie and Williamson 2010).

From a management perspective, it is clear that active conservation—anti-poaching activities, constant monitoring of the gorillas, and maintenance of the size and integrity of the habitat—have been paramount to the gorillas’ survival. It has long been noted that the Virunga gorillas are a relict population (Watts 1983:25), one so small that it is extremely vulnerable to human disturbance, and it is perhaps time to acknowledge that this is no longer a wild population but a highly managed one. We should accept this fact when assessing the feasibility of interventions. Population growth rate is more affected by changes in survivorship than by fertility, so efforts to conserve mountain gorillas are best focused on improving survivorship (Robbins et al. 2011). In reality, besides treating injuries and managing disease, few interventions are possible, but if mountain gorillas are to continue to survive in such a volatile region, a hands-on approach that incorporates knowledge of socioecology and demographic processes is justified. The increasing human pressures on mountain gorillas have already prompted a reevaluation of veterinary intervention policy: for nearly 20 years, the policy had been to intervene only if an injury or disease was human induced or life threatening; in recent years, some potentially life-threatening cases have been treated even if they were not caused by humans (Cranfield et al. 2006). With respiratory disease outbreaks among the habituated groups becoming more frequent and leading to fatalities (Palacios et al. 2011; Ryan and Walsh 2011), perhaps this reevaluation should go further. After careful analysis of human pathogen spillover, safety and cost of possible interventions, and efficiency of mitigation measures, Ryan and Walsh (2011) concluded that the conservation community should pursue proactive vaccination of great apes as a conservation strategy. Too few of these great apes remain for us to be passive about disease and natural selection “running their course”.

9 Postscript

This study took place during a period of stability in the Karisoke gorilla population, ironically at a time when the lives of people in the region were in turmoil. In the 6 years from 1996 to 2001, only 1 silverback left one of the three Karisoke research groups; in a subsequent 6-year period, 2003–2008, 14 males dispersed from the same three groups, 11 of them to become solitary (Stoinski et al. 2009). There have also been group splits, new groups formed, infant mortality through infanticide, and a high number of female transfers (Vecellio 2008), marking the return to a social dynamic reminiscent of earlier decades. The Karisoke gorillas seem to have been able to adapt to the prevailing social conditions, showing behavioral flexibility with their shifting reproductive strategies.

10 Parallels Between Gorillas and Cetaceans

All whales are listed by the Convention on International Trade in Endangered Species (CITES ), meaning that legal trade and products derived from them are highly controlled. In contrast, there is no legal exploitation of mountain gorillas. They are totally protected under national and international laws, on Appendix I of CITES, and it is forbidden to kill, capture, or harm them.

Both gorillas and cetaceans have low rates of reproduction and population growth. Slow demographic recovery stems from their life histories, such as a relatively long delay before first reproduction and long interbirth intervals. Actual growth rate in the Virunga gorilla population has been 1.15 % per year, well below the projected 3.8 % under ideal conditions (Gray et al. 2009).

There are similarities in population responses to legal (some cetaceans) and illegal (gorillas) hunting, as social balance in these complex mammals is easily disrupted. Their population structure is sensitive to the removal of older individuals, which may lead to fragmentation of social units. Lack of resilience to exploitation in cetaceans equates with the gorillas’ vulnerability to illegal killing. Trophy hunting that selectively removed silverback gorillas—key group members—and the killing of adults to capture infant gorillas have led to group disintegrations and subsequent deaths by infanticide (Kalpers et al. 2003). Similarly, in some cetaceans, direct removals have disrupted social structure.

To conclude, management interventions must take demographic processes into account and be fully cognizant of the disproportionately large impact of removing key individuals from these socially complex mammalian populations.