Female Mountain Gorillas Research Articles

Female age and reproductive stage influence copulation patterns in mountain gorillas’ variable mating system

Variation in mating systems and in individuals’ copulation patterns can have important consequences for the genetic structure of a population and ultimately its evolution. Whilst most gorilla sub-species form single-male, polygynous reproductive groups, mountain gorillas have both single-male and multimale reproductive groups. Considerable research has investigated the mating patterns of males in these multimale groups, but comparatively little is known about females. We investigated the copulation patterns of 71 female mountain gorillas over 13 years. We found that most sexually active, fecundable females in multimale groups had multiple mating partners. Females’ copulation patterns varied based on their reproductive stage, mating most often and with the greatest number of partners when they were pregnant, and least often when they had young dependent offspring. Females copulated throughout pregnancy, with pregnant females copulating more frequently in single-male groups than in multimale groups. Mating also varied with age, with older females mating less often and with fewer partners. Our findings confirm that when females transfer between single-male and multimale groups, they predominantly switch from copulating with one male to copulating with multiple males, and that females are also flexibly adjusting their copulation patterns across their lifetimes. This highlights the considerable variability of the mountain gorillas mating system, particularly from the female perspective, and the importance of accounting for within-species variation in copulation patterns.Significance statementPatterns of mating can vary both between individuals of the same species and within individuals across their lives. These patterns influence the genetic structure of a population. By examining copulation patterns in female mountain gorillas, we demonstrate that whilst females in single-male groups have only one mating partner, females in multi-male groups predominantly have multiple partners across a year. They also alter their copulation patterns across their lifetimes, copulating less often and with fewer partners as they age, and copulating most when pregnant. Our results highlight the flexibility with which female mountain gorillas can adjust their copulation patterns across their lifetimes, as the costs and benefits of copulation shift.

The dispersal dilemma among female mountain gorillas: Risk infanticide and gain protection

The dispersal dilemma among female mountain gorillas: Risk infanticide and gain protection

Dominance rank but not body size influences female reproductive success in mountain gorillas.

According to life history theory, natural selection has shaped trade-offs for allocating energy among growth, reproduction and maintenance to maximize individual fitness. In social mammals body size and dominance rank are two key variables believed to influence female reproductive success. However, few studies have examined these variables together, particularly in long-lived species. Previous studies found that female dominance rank correlates with reproductive success in mountain gorillas (Gorilla beringei beringei), which is surprising given they have weak dominance relationships and experience seemingly low levels of feeding competition. It is not currently known whether this relationship is primarily driven by a positive correlation between rank and body size. We used the non-invasive parallel laser method to measure two body size variables (back breadth and body length) of 34 wild adult female mountain gorillas, together with long-term dominance and demography data to investigate the interrelationships among body size, dominance rank and two measures of female reproductive success (inter-birth interval N = 29 and infant mortality N = 64). Using linear mixed models, we found no support for body size to be significantly correlated with dominance rank or female reproductive success. Higher-ranking females had significantly shorter inter-birth intervals than lower-ranking ones, but dominance rank was not significantly correlated with infant mortality. Our results suggest that female dominance rank is primarily determined by factors other than linear body dimensions and that high rank provides benefits even in species with weak dominance relationships and abundant year-round food resources. Future studies should focus on the mechanisms behind heterogeneity in female body size in relation to trade-offs in allocating energy to growth, maintenance and lifetime reproductive success.

Infant handling by female mountain gorillas: Establishing its frequency, function, and (ir)relevance for life history evolution.

Infant handling describes cases in which youngsters are temporarily removed from the care of their mothers and "taken care of" (held, carried, etc.) by other conspecifics. Handlers may gain indirect fitness benefits from these actions and can practice mothering skills, thereby improving the odds of survival of their own infants. Great apes are notable for displaying little infant handling. Apart from anecdotal observations, no published data exist on infant handling in wild mountain gorillas. We tested two of the most pertinent explanations ("kin selection" and "learning to mother") in a wild population of mountain gorillas in Rwanda. We predicted that (a) nulliparous females would exhibit infant handling (i.e., carrying) more than parous females and (b) maternal kin would exhibit more infant handling than nonkin. We collated 8 years of data on infant carrying behavior collected in 13 groups monitored by the Dian Fossey Gorilla Fund's Karisoke Research Center. Infant handling is an infrequent behavior (1,783 instances over 25,600 observation hours). A strong positive effect of relatedness and handler parity on the frequency of infant handling emerged. While the nature of handler-infant interactions (affiliative, abusive, etc.) remains unstudied, they could constitute alloparental care and could therefore attenuate maternal energetic burden and ultimately allow increased birth rates. However, the rarity of this behavior makes it an unlikely contributor to mountain gorillas' relatively short interbirth intervals.

Mothers may shape the variations in social organization among gorillas.

When mothers continue to support their offspring beyond infancy, they can influence the fitness of those offspring, the strength of social relationships within their groups, and the life-history traits of their species. Using up to 30 years of demographic data from 58 groups of gorillas in two study sites, this study extends such findings by showing that mothers may also contribute to differences in social organization between closely related species. Female mountain gorillas remained with their sons for significantly longer than western gorillas, which may explain why male philopatry and multimale groups are more common among mountain gorillas. The presence of the putative father and other familiar males did not vary significantly between species, and we found only limited support for the socio-ecological theory that the distribution of adult males is influenced by the distribution of females. Within each gorilla species, variations in those distributions may also reflect the different stages in the typical life cycle of a group. Collectively, our results highlight the potentially far-reaching consequences of maternal support that extends beyond infancy, and they illustrate the opportunity to incorporate additional factors into phylogenetic analyses of variations in social organization, including studies of human evolution.

Homosexual Behavior in Female Mountain Gorillas: Reflection of Dominance, Affiliation, Reconciliation or Arousal?

Humans are unique among primates for not only engaging in same-sex sexual acts, but also forming homosexual pair bonds. To shed light on the evolutionary origins of homosexuality, data on the occurrence and contexts of same-sex behavior from nonhuman primates may be of particular significance. Homosexual behavior involving females is poorly researched in most primate taxa, exceptions being Japanese macaques, rhesus macaques, Hanuman langurs and bonobos. We present data on homosexual behavior in female mountain gorillas in the Virunga Volcanoes (Rwanda) and test four functional hypotheses, namely reconciliation, affiliation, dominance expression and sexual arousal. Homosexual interactions between females involved both ventro-dorsal and ventro-ventral copulations accompanied by vocalizations and courtship displays. The only sociosexual hypothesis that received partial empirical support is the social status hypothesis, i.e., that mounting reaffirms the dominance hierarchy. There is also some limited evidence that same-sex behavior reflects an overall state of arousal or is triggered via a ‘pornographic’ effect. An adaptive function of female homosexual behavior is not readily apparent, and we tentatively conclude (until a more rigorous test becomes available) that it may simply be related to sexual gratification or that it is an evolutionary by-product of an adaptation.

Endocrine assessment of ovarian cycle activity in wild female mountain gorillas (Gorilla beringei beringei)

Variability of fertility (i.e. number of births per female per year) has been reported in females of many primate species but only a few studies have explored the associated physiological and behavioral patterns. To investigate the proximate mechanisms of variability in fertility of wild female mountain gorillas (Gorilla beringei beringei), we quantified the occurrence of ovulation, matings, and successful pregnancies among females. We examined the profiles of immunoreactive pregnanediol-3-glucuronide (iPdG) for sixteen females (seven nulliparous and nine parous females, including one geriatric female; average sampling period for fecal sample collection and behavioral observations per female=175days; SD=94days, range=66–358days) monitored by the staff of the Dian Fossey Gorilla Fund's Karisoke Research Center in Parc National des Volcans, Rwanda. We quantified ovarian cycles from iPdG profiles using an algorithm that we developed by adjusting the method of Kassam et al. (1996) to the characteristics of ovarian cycle profiles based on fecal hormone measurements. The mean length of ovarian cycles was 29±4days (median: 28days, N=13cycles), similar to ovarian cycle lengths of other great apes and humans. As expected, we found that female mountain gorillas exhibit longer follicular phases (mean±SD: 21±3days, N=13cycles) than luteal phases (mean±SD: 8±3days, N=13cycles). We also found that the frequency of ovarian cycles was greater in parous females (i.e. 20 ovarian cycles across 44 periods of 28days; 45.5%) than in nulliparous females (i.e. two ovarian cycles across 34 periods of 28days; 6%). However, the frequency of days on which matings were observed did not differ significantly between parous and nulliparous females, nor between pregnant and non-pregnant females. Five pregnancies were detected with iPdG levels, but only three resulted in live births, indicating miscarriages of the other two. In sum, this study provides information on the underlying endocrine patterns of variation in fertility depending on parity, mating behavior, and pregnancy success in a critically endangered great ape.

Causes, mechanisms, and consequences of contest competition among female mountain gorillas in Rwanda

Socioecological models predict that contest competition will arise when high quality foods can be usurped or monopolized, leading to more favorable energy balances and higher reproductive success for high-ranking females. Gorillas are interesting species for studying such predictions due to the variety of ecological conditions that they experience in different locations. Using data from 23 female mountain gorillas in 3 social groups in the Virunga Massif, we examined food characteristics that may influence contest competition (food site residence times [FSRT]), proximate mechanisms of such competition (aggression and avoidance), and potential consequences of competition (rank-related differences in energy intake rates, travel expenditures, and activity budgets). The average FSRT of each female was significantly correlated with dominance rank, which suggests that high-ranking females may have greater access to foods that are easier to usurp (as predicted with contest competition). High-ranking females were significantly more aggressive than low-ranking females, and both aggression and avoidance were significantly higher while feeding than during other activities. Contrary to predictions for contest competition, however, rank was not significantly correlated with energy intake rates nor with the proportion of time spent traveling versus feeding. Thus, we did not find any energetic benefits to explain why high-ranking females had significantly higher reproductive success in earlier studies. We propose several alternative explanations and discuss the potential complications of assessing contest competition in species with weak dominance relationships.

Tool use for food acquisition in a wild mountain gorilla (Gorilla beringei beringei).

On May 14, 2013, a wild, human-habituated, juvenile female mountain gorilla (Gorilla beringei beringei) in Volcanoes National Park, Rwanda was observed utilizing a tool to acquire food. The young gorilla watched an adult male use his hand to collect ants from a hole in the ground, and then quickly withdrew his hand and move away from the hole, shaking his arm to presumably remove biting ants. The juvenile female engaged in similar behavior, withdrawing her hand covered in ants, and shaking her arm vigorously. She then selected a piece of wood approximately 20 cm long and 2 cm wide at one end, 1 cm wide at the other, and proceeded to insert the stick into the hole, withdraw the stick, and then lick ants off of the stick. In contrast to the sizeable body of literature on tool use in wild chimpanzees, this is the first report of tool use for food acquisition by a wild gorilla.

Proximate mechanisms of contest competition among female Bwindi mountain gorillas (Gorilla beringei beringei)

Socioecological models provide a framework for predicting how animals respond competitively to the abundance and distribution of food resources. Testing predictions of socioecological models requires analysis of relationships among food resource characteristics, competitive behaviors, and measures of rank-related skew in energy balance or reproductive success. A positive relationship between dominance rank and energy balance has been observed among female mountain gorillas in Bwindi Impenetrable National Park, Uganda. This study examines the proximate mechanisms underlying feeding competition among those females. To assess the contestability of food resources, we measured the time a female spent feeding at a food site (food site residence time). We also examined the relationship between dominance rank and the access to resources, as well as the rate, context, and direction of aggression, and the number of neighbors in close proximity. As predicted, females had longer food site residence times and higher aggression rates with fruit and decaying wood than with herbaceous vegetation, suggesting that those resources may be contestable. Aggression was predominantly directed down the dominance hierarchy, although against expectation, rank was not significantly correlated with aggression rates or the time spent feeding on contestable foods. Higher-ranking females had significantly fewer neighbors, suggesting that lower-ranking females avoid higher-ranking ones. This study provides additional support for the claim that there is variability in how primates respond to the quality and distribution of food resources and that avoidance as a strategy to cope with feeding competition may result in similar skew in energy balance as rank-related aggression.

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.

Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas

Maintaining a balanced energy budget is important for survival and reproduction, but measuring energy balance in wild animals has been fraught with difficulties. Female mountain gorillas are interesting subjects to examine environmental correlates of energy balance because their diet is primarily herbaceous vegetation, their food supply shows little seasonal variation and is abundant, yet they live in cooler, high-altitude habitats that may bring about energetic challenges. Social and reproductive parameters may also influence energy balance. Urinary C-peptide (UCP) has emerged as a valuable non-invasive biomarker of energy balance in primates. Here we use this method to investigate factors influencing energy balance in mountain gorillas of the Virunga Volcanoes, Rwanda. We examined a range of socioecological variables on energy balance in adult females in three groups monitored by the Karisoke Research Center over nine months. Three variables had significant effects on UCP levels: habitat (highest levels in the bamboo zone), season (highest levels in November during peak of the bamboo shoot availability) and day time (gradually increasing from early morning to early afternoon). There was no significant effect of reproductive state and dominance rank. Our study indicates that even in species that inhabit an area with a seemingly steady food supply, ecological variability can have pronounced effects on female energy balance.

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.

Monitoring ovarian cycle activity via progestagens in urine and feces of female mountain gorillas: A comparison of EIA and LC–MS measurements

Understanding the reproductive biology of endangered mountain gorillas (Gorilla beringei beringei) is essential for optimizing conservation strategies, determining any demographic impact of socioecological changes, and providing information for comparative studies of primates. Non-invasive techniques have been used to assess the reproductive function of many primates and the importance of validating the measurements of hormones metabolites is widely recognized because they may vary even within closely related species. To determine if it is possible to non-invasively monitor ovarian activity in wild mountain gorillas, we used enzyme immunoassays (EIA) to quantify both urinary and fecal excretion of immunoreactive pregnanediol-3-glucuronide (iPdG), defined as all metabolites detected by a pregnanediol-3-glucuronide immunoassay (PdG EIA). Simultaneously, we performed the liquid chromatography mass spectrometry (LC-MS) to quantify the excretion of pregnanediol in urine and feces. Samples were analyzed over nine cycles of five females from the habituated gorillas monitored by Karisoke Research Center, Rwanda. As an additional indicator for ovulation timing, estrone conjugates (E1C) were measured in a subset of urine samples. The concentrations of iPdG and pregnanediol measured in the same samples were significantly correlated. Urinary concentrations of iPdG and pregnanediol fluctuated over the menstrual cycle but did not reveal any cyclic pattern, whereas a typical preovulatory urinary E1C surge and postovulatory increases of fecal iPdG and pregnanediol were detected. The luteal peaks of iPdG and pregnanediol levels in feces were on average 2.8 and 7.6 times higher, respectively, than averaged levels in the corresponding follicular phase. The relative number of days with observed matings was higher within the presumed fertile window than in the preceding period. Overall, the results indicate that fecal analysis of iPdG and pregnanediol is suitable for detecting ovulation in female mountain gorillas. Urinary measurements using both EIA and LC-MS appeared to be uninformative for monitoring ovarian activity in this primate.

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.

Infanticide and social flexibility in the genus Gorilla

Based on the cases of infanticide by male mountain gorillas reported from the Virunga volcanic region, the socioecological and life history features of gorillas satisfy the conditions for which infanticide may be expected. However, there are considerable variations in the occurrence of infanticide between habitats. We analyze the recent reports of infanticides that were directly observed or are suspected based on field evidence in two populations of eastern and western lowland gorillas (Kahuzi and Mbeli Bai, respectively) along with previous reports on mountain gorillas, and consider which social features are linked with and which factors influence the occurrence of infanticide in the gorilla populations. All victims were suckling infants and most of them were killed by males who seemed unrelated to them. Dependent infants are most vulnerable to infanticide when the protector male (its putative father in most cases) is absent, and so male protection ability seems to be important in determining female transfer decisions. Two cases observed in Kahuzi suggest that the infanticidal male may discriminate between infants to accept and those to kill according to his previous interactions with their mothers. Mating for a prolonged period prior to parturition is necessary for immigrant females to avoid infanticide by the new male of the group that they join. Infanticide was usually associated with female transfer, and the patterns of female association at transfer may shape variations in social structure between populations. Female mountain gorillas prefer large groups with multiple males and tend to transfer alone in order to seek more protection against infanticide in Virunga. By contrast, female eastern and western lowland gorillas tend to transfer with other females to small groups or solitary males, and maturing silverbacks take females to establish new groups through group fission in Kahuzi and Mbeli Bai. These differences may result in more multi-male and larger groups in the Virungas than in Kahuzi and Mbeli Bai. Rapid changes in density of gorilla social units and their relations following drastic environmental changes caused by recent human disturbances may also increase the probability of infanticide.

‘Infinite Loneliness’: the life and times of Miss Congo

The arrival of Miss Congo, a female mountain gorilla, in America provided the opportunity for a scientific study of the mental abilities of our close cousin. Since the mid-nineteenth century, gorillas had captivated the imagination of the public and scientific community alike. In 1925, psychobiologist Robert Mearns Yerkes was thrilled to gain access to such a rare primate specimen. Yerkes' study of 'The Mind of a Gorilla' reveals how our enduring fascination with the gorilla is driven by conflicting desires to demonstrate our connection with and distance from our fellow great apes.

A Novel Food Processing Technique by a Wild Mountain Gorilla (Gorilla beringei beringei)

Innovation, the invention of new behavior, has been observed in wild primates only infrequently. The processing of thistle (Cardus nyassanus) has previously been described as being one of the most complex food processing techniques used by mountain gorillas (Gorilla beringei beringei). We report a case of innovation in thistle leaf processing by a subadult female mountain gorilla in Bwindi Impenetrable National Park, Uganda. This technique involved rolling the thistle leaves into a ball between her palms prior to putting them in her mouth, as opposed to the standard method of folding leaves. All other weaned individuals (n = 13) were observed to use the standard method to process thistle leaves as described in Byrne et al. While the subadult female emigrated out of the research group 6 months after she had first been observed using the innovative technique, preventing observations of possible transmission within the group, it adds to the debate of whether food processing techniques used by gorillas are socially learned or not.

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.