Martha M. Robbins

Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method

Genetic analysis using noninvasively collected samples such as faeces continues to pose a formidable challenge because of unpredictable variation in the extent to which usable DNA is obtained. We investigated the influence of multiple variables on the quantity of DNA extracted from faecal samples from wild mountain gorillas and chimpanzees. There was a small negative correlation between temperature at time of collection and the amount of DNA obtained. Storage of samples either in RNAlater solution or dried using silica gel beads produced similar results, but significantly higher amounts of DNA were obtained using a novel protocol that combines a short period of storage in ethanol with subsequent desiccation using silica.

Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution

Fossils and molecular data are two independent sources of information that should in principle provide consistent inferences of when evolutionary lineages diverged. Here we use an alternative approach to genetic inference of species split times in recent human and ape evolution that is independent of the fossil record. We first use genetic parentage information on a large number of wild chimpanzees and mountain gorillas to directly infer their average generation times. We then compare these generation time estimates with those of humans and apply recent estimates of the human mutation rate per generation to derive estimates of split times of great apes and humans that are independent of fossil calibration. We date the human–chimpanzee split to at least 7–8 million years and the population split between Neanderthals and modern humans to 400,000–800,000 y ago. This suggests that molecular divergence dates may not be in conflict with the attribution of 6- to 7-million-y-old fossils to the human lineage and 400,000-y-old fossils to the Neanderthal lineage.

A demographic analysis of male life history and social structure of mountain gorillas

Twenty-five years of demographic data on free-ranging mountain gorillas (Gorilla gorilla beringei) from the Karisoke Research Center, Rwanda were used to assess male life histories and the variation within the age-graded social structure. Group types include lone silver-backs, one-male, multimale, and all-male groups. Although 60% of gorilla groups in the Virunga population are one-male, a multimale structure may increase chances of survival and future reproductive success for males at three stages of their lives. Infants born in one-male groups appear more likely to die from infanticide than those in multimale groups. Immature males in one-male groups may face decreased future reproductive opportunities compared to males in multimale groups. Adult males in one-male groups lack possible partners for coalition formation during intergroup encounters. Demographic constraints, such as length of time to male maturation, coupled with intense male-male competition for mates may limit the number and duration of groups with a multimale structure. Individuals are not restricted to one group type for their entire adult lives and males that attain maturity in each group type may eventually reproduce. Variation in male reproductive success is based both on length of reproductive tenure and on the number of mates.

Mountain gorillas: Three decades of research at Karisoke

1. Mountain gorillas of the Virungas: a short history Kelly J. Stewart, Pascale Sicotte and Martha M. Robbins Part I. Variation in the Social System of Gorillas: 2. Variation in the social system of mountain gorillas: the male perspective Martha M. Robbins 3. Female mate choice in mountain gorillas Pascale Sicotte 4. Dispersal patterns, group structure and reproductive parameters of eastern lowland gorillas at Kahuzi in the absence of infanticide Juichi Yamagiwa and Alastair McNeilage Part II. Within-group Social Behaviour: 6. Development of infant independence from the mother in wild mountain gorillas Alison Fletcher 7. The social relationships of immature gorillas and silverbacks Kelly J. Stewart 8. Social relationships of female mountain gorillas David P. Watts 9. Vocal relationships of wild mountain gorillas A. H. Harcourt and Kelly J. Stewart Part III. Feeding Behaviour: 10. Diet and habitat use of two mountain gorilla groups in contrasting habitats in the Virungas Alastair McNeilage 11. Clever hands: the food processing skills of mountain gorillas Richard W. Byre Part IV. Conservation and Management of Mountain Gorillas: 12. Assessment of reproduction and stress through hormone analysis in gorillas Nancy Czekala and Martha M. Robbins 13. Clinical medicine, preventive health care and research on mountain gorillas in the Virunga volcano region Anthony B. Mudakikwa, Michael R. Cranfield, Jonathon M. Sleeman and Ute Eilenberger 14. Conservation oriented research in the Virunga region Andrew J. Plumptre and Elizabeth A. Williamson 15. Status of the Virunga mountain gorilla population H. Dieter Steklis and Netzin Gerald-Steklis Afterward: Mountain gorillas at the turn of the century Bill Weber and Amy Vedder.

Complex tool sets for honey extraction among chimpanzees in Loango National Park, Gabon

Homo faber was once proposed as a label for humans specifically to highlight their unique propensity for tool use. However, new observations on complex tool use by the chimpanzees of Loango National Park, Gabon, expand our knowledge about tool-using abilities in Pan troglodytes. Chimpanzees in Loango, when using tools to extract honey from three types of bee nests, were observed to regularly use three- to five-element tool sets. In other words, different types of tools were used sequentially to access a single food source. Such tool sets included multi-function tools that present typical wear for two distinct uses. In addition, chimpanzees exploited underground bee nests and used ground-perforating tools to locate nest chambers that were not visible from the ground surface. These new observations concur with others from Central African chimpanzees to highlight the importance of honey extraction in arguments favoring the emergence of complex tool use in hominoids, including different tool types, expanded tool sets, multifunction tools, and the exploitation of underground resources. This last technique requires sophisticated cognitive abilities concerning unseen objects. A sequential analysis reveals a higher level of complexity in honey extraction than previously proposed for nut cracking or hunting tools, and compares with some technologies attributed to early hominins from the Early and Middle Stone Age. A better understanding of similarities in human and chimpanzee tool use will allow for a greater understanding of tool-using skills that are uniquely human.

A preliminary investigation of urinary testosterone and cortisol levels in wild male mountain gorillas

Urinary steroid hormone levels were measured in wild male mountain gorillas (Gorilla gorilla beringei) to determine how levels of testosterone and cortisol corresponded with age and social rank. Urine samples were collected noninvasively from 18 males, ranging in age from 3–26 years, in three groups of wild mountain gorillas at the Karisoke Research Center, Rwanda, Africa, and samples were analyzed using radioimmunoassay procedures. Males were classified as being immature (<7 years), maturing (10–13 years), or adult (+13 years of age). Immature males had significantly lower levels of testosterone and higher levels of cortisol than both maturing and adult males. No differences in testosterone or cortisol levels were found between maturing and adult males. Dominant males exhibited a trend toward significantly higher levels of testosterone than subordinate males, but no difference was found between cortisol levels of dominant and subordinate males. These results suggest that the increase in testosterone associated with puberty occurs prior to any outward sign of development of secondary sexual characteristics. Within‐group male–male competition may affect testosterone levels, but the lack of difference in cortisol levels between dominant and subordinate males suggests that subordinate males are not socially stressed, at least as measured by cortisol. Am. J. Primatol. 43:51–64, 1997.

Gorillas in the crossfire: population dynamics of the Virunga mountain gorillas over the past three decades

Small populations are particularly susceptible to disturbance. Routine censusing to monitor changes is important for understanding both population dynamics and the effectiveness of conservation strategies. Mountain gorillas Gorilla beringei beringei in the Virunga Volcanoes region of Rwanda, Uganda and the Democratic Republic of Congo have been censused five times since 1970. However, due to war and political unrest in the region since 1990, no census had been conducted since 1989, when the population was thought to number 324 gorillas. In 2000 we estimated population size using repeated observations of 17 habituated groups and information on 15 unhabituated groups obtained during patrols. The minimum population was 359 gorillas, and a best-case scenario correcting for groups that might not have been counted was 395. Using the minimum population and best-case scenario respectively, this represents a 0.9% or 1.8% annual growth rate over the last decade and 1.0% or 1.3% annual growth rate since 1972. This is lower than growth estimates made in several population viability analyses, but approximately 5% of the 1989 population is known to have died due to military activity over the last decade. Different subsets of the population exhibited different responses to disturbance caused by war. We discuss conservation strategies that are likely to have contributed to an increase in the gorilla population during this time of turmoil. While the population has grown, the results should be viewed with caution, not only because all known growth during the last decade can be attributed to one subset of the population, but also because the region is still plagued by political unrest.

Dietary Variability of Mountain Gorillas in Bwindi Impenetrable National Park, Uganda

Data on intraspecific dietary variability has important implications for understanding flexibility in foraging behavior, habitat utilization, population dynamics, and social behavior and may also assist in conservation efforts. We compared food availability and diet of a group of mountain gorillas (Gorilla beringei beringei) at a high altitude site and 2 groups at a low altitude site in Bwindi Impenetrable National Park, Uganda, from September 2001 to August 2002. Plant species diversity was greater at the low altitude site than at the high altitude site. The two groups at the low elevation consumed more plant species (140 species vs. 62 species), and a greater number of fruit species per mo (7 vs. 3 species) and per yr (36 vs. 11 species) than the high altitude group did. Furthermore, each group shared <51% of important fibrous food items in their diet with the 2 other groups. There is no significant difference in the proportion of days fruit remains were found in the dung among groups. Finally, according to Ivlevs electivity index, all groups positively selected the majority of food items in their diets. We attribute a large proportion of dietary variation between locations to differences in fruit availability and plant species composition between sites. Differences between groups at the low altitude site may be due to variation in food profitability—more profitable foods available to choose in the same area—within their overlapping home range, or group traditions. A comparison of our results with the diets of gorillas of the Virunga Volcanoes in Rwanda and Kahuzi-Biega, DRC shows that eastern gorilla populations have highly variable dietary patterns with limited overlap in species consumed among groups and populations.

Home range and frugivory patterns of mountain gorillas in Bwindi Impenetrable National Park, Uganda

Mountain, western, and Grauers gorillas exhibit broad differences in ecological patterns with western gorillas eating more fruit and having larger home ranges than their largely folivorous counterparts in the Virunga Volcanoes. We studied the home range and frugivory patterns of one group of Gorilla beringei beringei in the little-studied population of Bwindi Impenetrable National Park, Uganda, to compare with other populations and to investigate whether there was any relationship between patterns of frugivory and home range size. During the 3-year study, the gorillas ate 16 species of fruit on 27% of observation days. There was high variability in frugivory among the 3 years and no consistent seasonal pattern. Annual home range size was ca. 21 km2 for Years 1 and 2, and it increased dramatically to 40 km2 in Year 3. Home range size varied considerable between months and seasons, but there is no clear relationship between occurrence of fruit-eating and home range size. The group exhibited more fruit-eating and a larger home range size those ofthe gorillas in the Virunga Volcanoes. Their home range size is comparable to that of western gorillas, though Bwindi gorillas consumed less fruit. Home range size and utilization by all gorillas probably depends on a complex relationship between the distribution and abundance of both fruit and herbaceous vegetation and social factors such as male mating tactics.

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.