Andrew M. Robbins

Socioecological influences on the reproductive success of female mountain gorillas (Gorilla beringei beringei)

Over the past few decades, socioecological models have been developed to explain the relationships between the ecological conditions, social systems, and reproductive success of primates. Feeding competition, predation pressures, and risk of infanticide are predicted to influence how female reproductive success (FRS) depends upon their dominance rank, group size, and mate choices. This paper examines how those factors affected the reproductive success of female mountain gorillas (Gorilla beringei beringei) of the Virunga Volcanoes, Rwanda from 1967–2004. Reproductive success was measured through analyses of interbirth intervals, infant survival, and surviving infant birth rates using data from 214 infants born to 67 females. Mountain gorillas were predicted to have “within-group scramble” feeding competition, but we found no evidence of lower FRS in larger groups, even as those groups became two to five times larger than the population average. The gorillas are considered to have negligible “within-group contest” competition, yet higher ranked mothers had shorter interbirth intervals. Infant survival was higher in multimale groups, which was expected because infanticide occurs when the male dies in a one-male group. The combination of those results led to higher surviving birth rates for higher ranking females in multimale groups. Overall, however, the socioecological factors accounted for a relatively small portion of the variance in FRS, as expected for a species that feeds on abundant, evenly distributed foliage.

Extreme Conservation Leads to Recovery of the Virunga Mountain Gorillas

As wildlife populations are declining, conservationists are under increasing pressure to measure the effectiveness of different management strategies. Conventional conservation measures such as law enforcement and community development projects are typically designed to minimize negative human influences upon a species and its ecosystem. In contrast, we define “extreme” conservation as efforts targeted to deliberately increase positive human influences, including veterinary care and close monitoring of individual animals. Here we compare the impact of both conservation approaches upon the population growth rate of the critically endangered Virunga mountain gorillas (Gorilla beringei beringei), which increased by 50% since their nadir in 1981, from approximately 250 to nearly 400 gorillas. Using demographic data from 1967–2008, we show an annual decline of 0.7%±0.059% for unhabituated gorillas that received intensive levels of conventional conservation approaches, versus an increase 4.1%±0.088% for habituated gorillas that also received extreme conservation measures. Each group of habituated gorillas is now continuously guarded by a separate team of field staff during daylight hours and receives veterinary treatment for snares, respiratory disease, and other life-threatening conditions. These results suggest that conventional conservation efforts prevented a severe decline of the overall population, but additional extreme measures were needed to achieve positive growth. Demographic stochasticity and socioecological factors had minimal impact on variability in the growth rates. Veterinary interventions could account for up to 40% of the difference in growth rates between habituated versus unhabituated gorillas, with the remaining difference likely arising from greater protection against poachers. Thus, by increasing protection and facilitating veterinary treatment, the daily monitoring of each habituated group contributed to most of the difference in growth rates. Our results argue for wider consideration of extreme measures and offer a startling view of the enormous resources that may be needed to conserve some endangered species.

Long-term dominance relationships in female mountain gorillas: Strength, stability and determinants of rank

Summary A common practice in studies of social animals is to rank individuals according to dominance status, which has been shown to influence access to limited resources and stability of social relationships, and may in turn correlate with reproductive success. According to the socioecological model for primates, most female dominance relationships are either nepotistic or virtually undetectable (egalitarian), with nepotistic species being philopatric, and dispersing females being egalitarian. Female mountain gorillas (Gorilla beringei beringei) disperse, and they have been characterized as being egalitarian, but previous studies have not examined their dominance relationships from a long-term perspective. We evaluated 15 matrices of displacement/supplantation interactions that spanned 30 years of observations in the Virunga Volcanoes region, and included 51 female mountain gorillas in six groups. Only 4% of displacements were directed against higher ranking females, and when matrices had less than 5% unknown dyads, linearity indices were consistently greater than 0.95. Therefore, previous results suggesting undetectable dominance relationships may have reflected an insufficient quantity of data for this species, rather than actual nonlinearity in its hierarchies. Dominance depended on age and group tenure rather than nepotism, yet some females maintained a high ranking for most of adulthood (15-25 years). Most rank shifts occurred through changes in group composition, rather than switches in established relationships. These results fit within growing evidence for linear individualistic hierarchies in some primates, often coupled with dispersal, as commonly found in ungulates. In light of these results, we propose that the dominance relationships of female mountain gorilla are best characterized as ‘Dispersal-Individualistic’ instead of the previously suggested ‘Dispersal-Egalitarian’.

Socioecological influences on the dispersal of female mountain gorillas—evidence of a second folivore paradox

Socioecological models indicate that the group structure and female dispersal patterns of primates are determined primarily by the abundance and distribution of food, predation pressures, and infanticide risks. In response to those influences, females of folivorous primates are considered relatively free to disperse into groups with the optimal size and structure. Yet some folivores live in small groups despite a potentially higher risk of predation, an apparent inconsistency known as the folivore paradox. This paper examines the female dispersal of a folivorous primate, the Virunga mountain gorillas. Mountain gorillas currently have no natural predators, but this species presents a different version of the folivore paradox: why do 50–60% of females reside in smaller one-male groups despite a higher risk of infanticide? In this study, females left one-male groups more frequently than multimale groups, but transfer destinations were not consistently biased toward multimale groups and those groups did not have higher immigration rates. We found no evidence of dispersal to avoid feeding competition within large groups, even as they have become three to five times larger than average. Thus, the lack of a consistent bias toward multimale groups was not because they are typically larger than one-male groups. Instead, the apparent inconsistencies may reflect limited female transfer opportunities, other influences on dispersal, and possibly an evolutionary disequilibrium in which current behavior does not optimize fitness.

Impact of male infanticide on the social structure of mountain gorillas

Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2–3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.

Lifetime reproductive success of female mountain gorillas

Studies of lifetime reproductive success (LRS) are important for understanding population dynamics and life history strategies, yet relatively little information is available for long-lived species. This study provides a preliminary assessment of LRS among female mountain gorillas in the Virunga volcanoes region. Adult females produced an average of 3.6 ± 2.1 surviving offspring during their lifetime, which indicates a growing population that contrasts with most other great apes. The standardized variance in LRS (variance/mean(2) = 0.34) was lower than many other mammals and birds. When we excluded the most apparent source of environmental variability (poaching), the average LRS increased to 4.3 ± 1.8 and the standardized variance dropped in half. Adult lifespan was a greater source of variance in LRS than fertility or offspring survival. Females with higher LRS had significantly longer adult lifespans and higher dominance ranks. Results for LRS were similar to another standard fitness measurement, the individually estimated finite rate of increase (λ(ind) ), but λ(ind) showed diminishing benefits for greater longevity.

Phenotypic correlates of male reproductive success in western gorillas

Sexual selection is thought to drive the evolution of sexually dimorphic traits that increase male reproductive success. Despite a large degree of sexual dimorphism among haplorhine primates, phenotypic traits that may influence the reproductive success of males are largely unstudied due to long life spans and the difficulties in quantifying such traits non-invasively. Here we employ digital photogrammetry of body length and crest size, as well as ranking of the gluteal muscle size, to test whether these sexually dimorphic traits are associated with long-term measures of male reproductive success in western gorillas. Among 19 adult male gorillas monitored for up to 12.5 years, we found that all three phenotypic traits were positively correlated with the average number of mates per male, but only crest size and gluteal muscle size were significantly correlated with offspring survival and the annual rate of siring offspring that survive to weaning age. We discuss why such sexually dimorphic traits might be under ongoing selection in gorillas and other species.

Leave or conceive: Natal dispersal and philopatry of female mountain gorillas in the Virunga volcano region

Natal dispersal is often attributed to inbreeding avoidance, competition for resources or competition for mates, but the patterns and frequency of dispersal vary considerably among and even within species. We examined the possible reasons for dispersal and philopatry of natal nulliparous female mountain gorillas, Gorilla gorilla beringei, in the Virunga volcano region, including comparisons with non-natal and/or parous females. Competition among females is generally weak and ineffective in this population, and inbreeding avoidance has been considered the ultimate cause of natal dispersal. Yet fewer than half of nulliparous females left their natal group when the dominant male was old enough to be their father, so they did not rely entirely upon dispersal to avoid such risk of inbreeding. Almost all natal nulliparous females were with at least one sexually active male who was not old enough to be their father, so the presence or absence of such mating alternatives also did not determine whether they left. Natal nulliparous females were more likely to leave groups with only one adult male, where infanticide losses have been higher than in multimale groups. Thus natal dispersal seemed to be influenced by infanticide avoidance, which has been considered the ultimate cause of secondary dispersal. Natal nulliparous females have more time to encounter suitable destinations than other females, which may be a proximate reason why they were more likely to transfer despite having the same ultimate cause of dispersal.

Does dispersal cause reproductive delays in female mountain gorillas

Summary Reproductive delays are a potential cost of dispersal, even when females transfer directly from one social unit to another. Delays may occur before a transfer if females avoid conception while waiting to encounter other groups, and delays following the transfer could be caused by greater stress or poorer nutrition in the new group. This paper examines the timing of reproduction and inter-group transfers of female mountain gorillas in the Virunga Volcano region in Africa. Reproductive delays were not observed for nulliparous females, who typically transfer more than a year before their first conception. For parous females, interbirth intervals were significantly longer when they contained a transfer, but limited observations did not suggest that females were avoiding conception while waiting to transfer, and immigrants did not take significantly longer to conceive than other females. We conclude that transfers may not delay reproduction of parous females, but conversely, dispersal may become more likely when successful reproduction is delayed for any reason (e.g., infertility, miscarriages, and infant mortality). We present a preliminary mathematical model to predict how much of a delay a transferring female could afford, if offspring mortality were reduced in her new group.

Dominance rank differences in the energy intake and expenditure of female Bwindi mountain gorillas

Socioecological models predict that contest competition for clumped foods can lead to higher energy intake and lower energy expenditure for higher-ranking individuals. Here, we examine the relationships between dominance rank and energy intake and expenditure of female mountain gorillas in Bwindi Impenetrable National Park, Uganda (Gorilla beringei beringei). Bwindi gorillas have weak dominance relationships, feed on nonreproductive plant parts throughout the year, and consume fruit when it is seasonally available. We used behavioral observations on one group of gorillas and nutritional analysis of their major food items to calculate energy intake rates and estimated energy expenditure. Using linear mixed models, we found a significant positive relationship between dominance rank and energy intake rates, due to higher-ranking females having faster ingestion rates, rather than consuming foods with higher energy concentrations. Lower-ranking females did not spend significantly more time feeding to compensate for their lower energy intake rates. Lower-ranking females spent significantly more time traveling than higher-ranking females, leading to a negative relationship between dominance rank and energy expenditure. The combined results revealed a significant positive relationship between dominance rank and energy balance. Higher-ranking females did not spend longer feeding on fruit than lower-ranking ones, and the relationship between dominance rank and energy intake rates was not stronger when fruit was available. According to socioecological models, these results suggest that contest competition may be occurring with both fruit and nonreproductive plant parts, which would be consistent with growing evidence that nonreproductive plant parts can be contestable.