Social relationships of immigrant and resident female mountain gorillas. I. Male-female relationships

Adult males are important social partners for all females in mountain gorilla social groups, but male-female relationships can vary in association with variation in female residence status, male age and mating status, and relatedness. Such variation occurred in a large group observed over a 3-year period. All females associated and interacted affiliatively relatively often with a young silverback with whom all mated. Long-term resident females also did so with an old, non-breeding male to whom most were related, but recent immigrants spent little time near him and had few non-aggressive interactions with him. The old male made agonistic interventions to support relatives; interventions in female conflicts by the younger male tended to ameliorate competitive differentials that immigrants faced and may have helped him to retain them as mates. Males aggression toward females was common, most probably served as a mating tactic, and did not involve resource competition. Extensive grooming by an adolescent male suggests that males may also use affiliative behavior to develop mating relationships. Females may have competed for proximity with and social access to the younger silverback; competitive success could influence how well females and their offspring are protected by silver-backs, but the extent of such competition was not clear. Large group size may have heightened differentiation of male-female relationships and competition among females, but comparative data from smaller groups generally corroborate the findings from the large group. © 1992 Wiley-Liss, Inc.     

Observations on the ontogeny of feeding behavior in mountain gorillas (Gorilla gorilla beringei)

This report describes observations on the ontogeny of food choice in mountain gorillas (Gorilla gorilla beringei), made during a 17-month field study of mountain gorilla feeding ecology in the Parc National des Volcans, Rwanda. Data are presented on the feeding behavior of two infants observed from birth to the age of 8 months and on older infants and juveniles. This information is compared with data on the composition and diversity of the diets of young adults and adults in the same social group. Initial feeding by infants is usually synchronized with the mother's behavior: infants ingest the same food, or a different part of the same plant species, currently being eaten by the mother or just eaten by her. This suggests that observational learning is largely responsible for the transmission of food preferences. Most feeding by young infants, whether or not synchronized with the mother's, is on those foods eaten most frequently by adults. Infants also independently sample potential foods, some of which are apparently not consumed by adults. The frequency of sampling declines with age, although even adults occasionally ingest foods not observed to be eaten by other adults. By the age of 3 years, young mountain gorillas have developed the basic dietary patterns of adults, in terms of the number of foods eaten, the proportions in which specific foods are consumed, and diet diversity and equitability. There is a strong possibility that chemical cues influence food choice, but their role remains unclear.     

Further developments in the breeding population of lowland gorillas at Apenheul

In 1987 a second group of lowland gorillas was formed at Apenheul. Aspects of the zoo-technical management (diet, accommodation, etc.) are described. The management and the development of the population, including mother-rearing of all offspring, are described. Special attention is given to the formation of a second group by introducing two zoo-born females and a non-breeding female from one group to a nonrelated male to form a second group. These transfers of group members resulted rather quickly in pregnancies. The two groups are housed on adjacent islands, and the advantages and disadvantages of such a facility are discussed.     

A preliminary study of selective visual attention in female mountain gorillas (Gorilla gorilla beringei)

Visually attending to conspecifics can give group-living primates important ecological information, help them to anticipate the behavior of others and to regulate interactions with them, and provide other valuable social information. Variation in the importance and quality of social relationships should influence the way individuals selectively attend to fellow group members. Preliminary data on visual monitoring of conspecifics by wild female mountain gorillas (Gorilla gorilla beringei) show that selective attention mirrors variation in social relationships. Social bonds between males and females are central to gorilla society; correspondingly, females are more likely to stop feeding, and focus their attention on males who walk into view than on females, especially when males give dislays. Females are more likely to focus on other females with whom they have antagonistic relationships than those (mostly close relatives) with whom they have affiliative, cooperative ones. Further research on the context and consequences of visual monitoring could help to address questions about the regulation of social relationships and about social cognition in gorillas.     

The influence of male mating tactics on habitat use in mountain gorillas (Gorilla gorilla beringei)

Previous research has shown that both ecological and social factors influence mountain gorilla habitat use. New data on habitat use by a male gorilla and by a group confirm that male mating competition influences short- and long-term habitat use patterns, and show that its influence can supersede that of ecological factors on a long-term basis. When solitary, the male regularly approached and sometimes followed groups. His monthly home range size and equitability of home range use were directly proportional to the number of such interactions per month. His relationships with other groups became more conservative after he gained females, and, contrary to expectations based on metabolic needs, he used a much smaller area. The group considered here gradually expanded its home range and shifted its areas of intensive use throughout a three-year period. It then made a complete home range shift after three dramatic interactions, during which it was temporarily fragmented and two females emigrated. The group shared its home range with many other social units; overlap with most of these decreased after the shift. The degree of overlap and the lack of site fidelity by males and their groups support the argument that transfer is not ecologically costly to mountain gorilla females.     

Social relationships of immigrant and resident female mountain gorillas,II: Relatedness,residence, and relationships between females

Female transfer is common in mountain gorillas, but most adult females reside with female relatives for at least some of their lives. In four mountain gorilla social groups, co-resident relatives had higher rates of affiliative interaction and lower rates of aggressive interaction, and were more tolerant of each other, than non-relatives. These differences were greater for maternal than for paternal relatives. Non-relatives typically had few affiliative interactions, but some (mostly but not entirely long-term co-residents) had friendly relationships. Females showed reciprocity in affiliative behavior. Long-term residents in two groups maintained less tolerant relationships with more recent immigrants than with each other and than did most pairs of immigrants. The effects of relatedness and residence status on relationships may sometimes be complementary because both factors can lead to similar reproductive interests. A potential exists for some resemblance between female-female social relationships in mountain gorillas and those in female-bonded primate species. However, even female relatives usually spend little time interacting socially with each other, and the benefits of relationships with males outweigh those of relationships with other females. © 1994 Wiley-Liss, Inc.     

Functional analysis of social staring behavior in an all-male group of mountain gorillas

A total 202 social staring episodes (prolonged gazing by one individual toward another within a short distance) were observed in various social contexts among six unrelated, adult, and subadult male mountain gorillas. Staring was not accompanied by distinct facial expressions by actors or recipients, irrespective of their age or dominance rank. Younger, subordinate animals tended to stare at elder, dominant animals more frequently than vice versa. Staring may have multiple functions depending on the social context. In the initiation of non-agonistic interactions, staring rarely occurred, but was very successful for younger males in eliciting play or homosexual interactions from older animals. Staring was also directed by younger males to older males for greeting or appeasement. It may possibly play a role in reducing the increased social tension that occurs during or after conflict and in averting the potential conflict among older males. Younger males occasionally supplanted older males by staring at feeding spots. This slow supplantation is similar to the phenomenon of food sharing achieved through begging behavior in chimpanzees and bonobos. A prolonged gaze including staring by subordinates towards dominants may characterize the frequent and prolonged face-to-face interactions in the African great apes, and contrasts with a frequent gaze aversion by subordinates towards dominants in macaques or baboons. A difference between gorillas and other apes is that, chimpanzees and bonobos make positive contact with each other through eye contact, while gorillas simply stare at another without physical contact in greeting or appeasement process. Staring may serve an effective strategy for younger male gorillas to intervene safely in olders' conflict and sometimes to suppress or inhibit olders' performance, but their non-agonistic contacts or supporting attacks may not contribute to the establishment or support of social bonds between them. It is possible that staring may be common among the African great apes and man, and that it has evolved as a tactics to mask the dominant/subordinate relationships between individuals with multiple functions.     

A case study of mother-son transfer in mountain gorillas

In mountain gorillas (Gorilla g. beringei), male immigration in bi-sexual units is rare. This paper presents the case of a nearly weaned male infant gorilla who followed his mother in her transfer. This case was recorded in the study population at the Kariske Research Center in 1988. The data come from observation in Group B (on 12 days just prior to the transfer and on 54 days after the transfer over a period of 6 months). The situation of the infant did match the conditions in which infanticide occurs in gorillas, but he was not killed, despite receiving male aggression and being wounded twice. In fact, both the mother and the infant received male aggression more frequently than the long term residents in the group. The aggression received by the mother decreased after she mated with the males and after she weaned the infant. The aggression received by the infant, however, did not decrease after his mother mated with the males, and increased in intensity. The infant reacted fearfully to male aggression, in marked contrast to his mother, who reacted either with indifference, or by simply avoiding the males. The aggression eventually stopped, and the infant became a blackback in Group B. Evolutionarily, the death of the infant would not have markedly accelerated the mother's return to estrus, but the death of the infant could still have benefitted the males, by decreasing the reproductive output of a competitor. Adult male gorillas are also presumably selected to resist male immigration. Proximately, the aggression directed towards the infant was not related to mating access to the mother. The sex of the infant may contribute to explain the post-transfer male aggression, but data on the integration of old female infants in a new group is needed to test whether the sex of the infant has an effect on their vulnerability to infanticide. Also, the intense fear displayed by the infant may have played a role in prompting male aggression.     

Complex leaf-gathering skills of mountain gorillas (Gorilla g. beringei): Variability and standardization

The skills that mountain gorillas use to deal with the stings, tiny hooks, and spines protecting common plant leaves in their diet were examined for variation within and between animals. Many elements of uni- and bimanual performance were identified, often involving delicate precision and coordination, and varying idiosyncratically, erch individual having a different set of preferred elements. Many of these elements are functionally equivalent, and all but one weaned animals showed full processing capability; the history of the one exception suggests that early experience with the task may be important. Gorillas' idiosyncrasy in manual skill elements is entirely consistent with trial-and-error learning at this level. By contrast, each individual uses very few techniques (structured sequences of elements) for most processing, and these techniques are the same across the population. Where animals deviate from this generalization, they largely employ the simpler technique normally used for undefended leaves. Lateralization increases from start to finish, consistent with a logical structure in which each stage has a laterality bias and each stage is sequentially dependent on the last. Variations from their commonest, techniques occur in all animals (on average, about nine variant techniques were recorded from each animal). The repertoire of techniques increases significantly with age, whereas the repertoire of elements does not. This points to an initial reliance on a single logical structuring that is well established by weaning (about 3.5 years), with subsequent development of the ability to vary the technique used so as to take advantage of variations in the environment. Standardization of logical organization, despite variability between different animals in individual elements and behavioral laterality, suggests that the logical ordering of elements and the interrelationships of processing stages is copied by program-level imitation. © 1993 Wiley-Liss, Inc.     

Seasonality in the Ecology and Life Histories of Mountain Gorillas (Gorilla gorilla beringei)

The abundance of food, especially that of fruit and often that of young leaves, varies considerably over time for most primates. This variation can depend on or be independent of seasonality in rainfall. Mountain gorillas (Gorilla gorilla beringei) in the Virungas are exceptional: their habitat contains almost no edible fruit, and they mostly eat perennially available herbs and vines that are densely and evenly distributed in much of their habitat. Earlier studies documented little consistent temporal variation in mountain gorilla diets and habitat use, except for seasonal use of bamboo by some groups, and documented no birth seasonality. Long-term data ( 7 years) on 6 mountain gorilla groups confirm these results for habitat use, except that they show some seasonality in use of the upper altitudinal extremes of the gorillas' home ranges for unclear reasons. Relatively low and inconsistent variation in habitat quality over time should lower the costs of grouping for gorillas compared to other apes. Long-term data also confirm the absence of seasonality in births and conceptions. However, they show that mortality rates and risk of respiratory infections vary directly with rainfall. These relationships are probably causal and may be mediated through thermoregulatory stress.     

Inter-group encounters and female transfer in mountain gorillas: Influence of group composition on male behavior

This paper examines the behaviors used by male gorillas (G. gorilla beringei) to influence female choice during inter-group encounters. Encounters are related to the acquisition of females rather than to the defense of a group's range. Data on 58 independent encounters confirms that encounters are generally aggressive, but that contact aggression is less frequent than previously reported. A high number of potential migrants in one of the groups involved, rather than the newness of either group, predicts the likelihood of contact aggression between males. Encounters with a newly formed unit last longer than encounters involving established groups. Male herding serves to prevent female transfer. Females without dependent offspring are more likely than others to be herded. Proceptive females are the target of herding more often than non-proceptive cycling females. Groups where herding has been observed are more likely to be newly formed, and they include significantly more males. This last result confirms that there are advantages to male cooperation in gorillas. It also raises the question of why such cooperation does not occur more often. © 1993 Wiley-Liss, Inc.     

Movement patterns of a group of free-ranging mountain gorillas (Gorilla gorilla beringei) and their relation to food availability

Relationships between the movement patterns of free-ranging mountain gorillas (Gorilla gorilla beringei) and the abundance and distribution of foods in their home range were examined. During an 18-month field study, the ranging of one group of G. gorilla beringei was recorded on a 250 × 250 m grid system, from which measurements of frequency and duration of use, travel rate, and rate of revisitation of each quadrangle by the group were derived. Food items were sampled in selected quadrangles throughout the home range and various measures of food abundance, frequency and diversity were calculated. Analyses based on both spatial and temporal variation in food availability give supporting evidence for the prediction that mountain gorilla ranging patterns are influenced by the distribution and abundance of foods. Quality of food appears to be an important factor, as shown in analyses of yearly patterns and monthly changes in ranging. The gorillas studied spent more time in the higher quality areas of their home range, responded to a correlate of decreasing food abundance by increasing their rate of travel and area used, and revisited regions more frequently when the renewal rate of foods was clearly greater. Each of their foraging tactics can be explained as serving to increase the efficiency of harvesting foods.     

Regurgitation and reingestion in captive gorillas: Description and intervention

Direct observation of regurgitation and reingestion (r/r) of captive gorillas was used to describe and catalog this behavior and thus lay the groundwork for possible intervention in the r/r cycle. Analysis of questionnaires regarding 117 gorillas at 17 zoos suggests that social deficits during early development contribute to the occurrence of r/r later in life. Wild-caught and captive-born, hand-reared gorillas show higher incidence of r/r than that of mother-reared infants. R/r increases the daily ingestion time. Feeding browse decreases r/r and increases time spent feeding from about 11% of the day to 27% of the day.     

Intestinal parasites and bacteria of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda

A survey in 1994 examined intestinal helminths and bacterial flora of mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda. Parasites and bacteria were identified to genus in the feces of two groups of tourist-habituated and one group of non-tourist-habituated mountain gorillas. Eggs were identified as those of an anoplocephalid cestode, and nematode eggs representative of the genera: Trichuris, Ascaris, Oesophagostomum, Strongyloides, and Trichostrongylus. This is the first report of Ascaris lumbricoides-like eggs in mountain gorillas. Fecal samples (n=76) from all groups contained helminth eggs, with strongyle eggs and anoplocephalid eggs being the most common. Salmonella and Campylobacter were found in both gorilla groups. Regular long-term non-invasive fecal monitoring of the populations of mountain gorillas is essential for the prevention and identification of potential health threats by intestinal parasites and bacteria in this highly endangered subspecies.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Determinants of female dispersal in Thomas langurs

Female dispersal occurs in a number of primate species. It may be related to: avoidance of inbreeding, reduction in food competition, reduction of predation risk, or avoidance of infanticide in combination with mate choice. Female dispersal was studied for a 5-year period in a wild population of Thomas langurs (Presbytis thomasi) that lived in one-male multi-female groups. Juvenile and adult individuals of both sexes were seen to disperse. Females appeared to transfer unhindered between groups, mostly from a larger group to a recently formed smaller one. They transferred without their infants and when not pregnant, and seemed to transfer preferentially during periods when extra-group males were harassing their group. During these inter-group encounters extra-group males seemed to try to commit infanticide. Thus, the timing of female transfer was probably closely linked to infanticide avoidance. Moreover, females seemed to transfer when the resident male of their group was no longer a good protector. The observations in the present study suggest that females transferred to reduce the risk of infanticide. Female dispersal may have another ultimate advantage as well, namely inbreeding avoidance. Due to the dispersal of both females and males the social organization of Thomas langurs was rather fluid. New groups were formed when females joined a male; male takeovers were not observed. Bisexual groups had only a limited life span, because all adult females of a bisexual group could emigrate. This pattern of unhindered female dispersal affects male reproductive strategies, and in particular it might lead to infanticidal behavior during inter-group encounters. Am. J. Primatol. 42:179–198, 1997. © 1997 Wiley-Liss, Inc.     

Age-related sperm transfer and sperm competitive ability in the male hide beetle

The influence of male age on reproductive success after a singlemating has been explored widely; however, few studies have investigatedwhether quantitative or qualitative differences in male spermare responsible for the observed patterns. Moreover, the roleof male age on sperm competitive ability has been largely ignored.We examined the importance of male age on the probability andamount of sperm transferred during a single mating and exploredwhether sperm competitive ability varies with male age in thehide beetle Dermestes maculatus, a species where sperm viabilitydoes not vary with male age. We also investigated whether spermtransfer rates varied with female age. We found that the probabilityof sperm transfer and the amount of sperm transferred variedwith male, but not female, age. All males performed behaviorallysuccessful copulations, but intermediate-age and old males weremore likely to transfer sperm successfully and also transferreda greater quantity of sperm than young males. Old males wereless likely to transfer sperm than intermediate-age males, butif they did transfer sperm successfully, they transferred comparableamounts. Sperm competitive ability varied with male age andreflected the quantity of sperm transferred. On average, intermediate-agemales achieved greater fertilization success when competingagainst young or old males than when competing against otherintermediate-age males. Old males were poor competitors againstintermediate-age males, but they achieved significantly higherrates of fertilization when competing against young males. Ourfindings suggest that quantitative differences in the amountof sperm transferred determine male success in sperm competitionin the hide beetle.     

Potential for female kin associations in wild western gorillas despite female dispersal

Female philopatry and male dispersal are the norm for most mammals, and females that remain in their natal region often derive foraging or social benefits from proximity to female kin. However, other factors, such as constraints on group size or a shortage of potential mates, may promote female dispersal even when female kin associations would be beneficial. In these cases, female kin associations might develop, not through female philopatry, but through female emigration to the same group. To date, little attention has been focused on the potential for kin-biased behaviour between females in female-dispersing species. Here we investigate the genetic relationships among adults in eight wild groups of unhabituated western gorillas (Gorilla gorilla) at the Mondika Research Center using microsatellite genotyping of DNA collected from hair and faeces. We found that almost half (40%) of adult females had an adult female relative in the same group and average within-group relatedness among females was significantly higher than that expected under a model of random dispersal. This provides the first genetic evidence that females can maintain social associations with female relatives in spite of routine natal and secondary dispersal. In addition, we show that females appear to avoid related silverback males when making dispersal decisions, suggesting that a strategy of non-random female dispersal may also function to avoid inbreeding.