Pascale Sicotte

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.

Influence of Human Food Consumption on the Time Budget of Vervets

In nonhuman primate groups that utilize crop and food-raiding strategies, the inclusion of human food in the diet can have a pervasive impact on the activity budget. Human food is usually of higher quality and energy per unit than wild food. Thus, metabolic demands may be reached sooner on a human food diet, which in turn leads to improved foraging efficiency. In particular, a reduction in time spent feeding is associated with an increase in time spent resting. We investigated changes in time budget in a group of vervets (Chlorocebus aethiops pygerthrus) living in a tourist and cultivated area of Entebbe, Uganda (Zoo group). Saj collected 123 hr of focal observations on 17 individuals. Human food constituted half of the diet of Zoo group. Access to human food resulted in a high proportion of time resting and a low proportion of time feeding. The group had a small average daily range and a small home range in relation to other reports on unprovisioned groups. The time budget differences suggest that the juveniles spent more time moving and feeding and less time resting than adults did, and that adult females were more social than adult males were. These patterns have been observed in both provisioned and unprovisioned vervet groups. In contrast to a report from an unprovisioned group (Harrison, 1983), lactating females in this provisioned situation were able to maintain feeding and activity levels similar to those of other adults. However, adult females spent significantly less time consuming human food than juveniles did. We suggest that the risk associated with human food consumption may explain the low consumption of human food by females with dependent offspring. The differences may also reflect the different nutritional requirements of lactating females or the tendency for juveniles to be more exploratory than other group members.

Effect of group size on activity budgets of Colobus vellerosus in Ghana

Group size influences foraging efficiency in several primates. We examined the activity budgets of 3 groups of Geoffroys pied colobus (Colobus vellerosus) at the Boabeng-Fiema Monkey Sanctuary in Ghana to determine whether larger group size induces scramble competition. We studied 2 groups (B1; N = 7-8 and WW; N = 31-33) occupying slightly overlapping home ranges from August to November 2000. We observed the third group, B2 (N = 15-16), comprising B1 and 7 male invaders in the same home range as B1 from August to November 2001. By comparing groups belonging to the same population and occupying sligthly overlapping or similar home ranges, we were able to control, to a certain extent, for differences in food distribution. We recorded a total of 3353 scans, yielding 14,886 activity records, over 73 days. As with other black-and-white colobus, resting was their most common activity (59%). Intergroup comparisons suggest that time spent feeding, resting and moving did not vary in relation to group size. However, intragroup comparisons between the sexes show that females in the large group spent more time feeding than males did, whereas this was not the case in the small group, which suggests that scramble competition may be occurring among female Colobus vellerosus at BFMS. It is also possible that this may be due to greater nutritional requirements because of a higher proportion of infants in the large group. In fact, the proportion is quite similar between the two groups, lending support to the idea that females in the two groups had comparable nutritional demands due to lactation. This suggests that increased feeding in females in the large group was partly an effect of scramble competition. Group size and group composition also influenced the frequency of social behavior. There was more grooming in the large group, and it was performed mostly by females. The distribution of activities throughout the day was similar to the pattern reported for other black-and-white colobus.

Female dispersal patterns in six groups of ursine colobus (Colobus vellerosus): infanticide avoidance is important

Summary Under the dispersal/foraging efficiency model, colobines are predicted to be ‘indifferent mothers’, neither facilitating philopatry for their daughters nor evicting them from the natal home range because food competition is thought to be slight. We observed six groups of Colobus vellerosus at the Boabeng-Fiema Monkey Sanctuary in Ghana (2000‐2007) and recorded changes in female composition caused by observed (N = 11) and inferred (N = 12) emigrations and immigrations (N = 3). We also observed 14 immigration attempts. Most emigrating females were subadult and nulliparous. Parallel emigration was frequent. Resident females behaved aggressively to immigrating females and immigration attempts were rarely successful. Voluntary female emigration (N = 10) occurred mostly when male group membership was unstable or in association with the immigration of all-male bands. Involuntary emigrations (N = 13) associated with increased female‐female aggression occurred in the two largest groups, where parous females targeted nulliparous maturing females. Larger groups tended to lose females and female immigration was successful only in the study group with the lowest number of females. Females appear to emigrate to reduce infanticide threat although feeding competition is reduced in smaller groups as well. C. vellerosus at BFMS are better described as ‘incomplete suppressors’.

Test of the ecological‐constraints model on ursine colobus monkeys (Colobus vellerosus) in Ghana

For group‐living mammals, the ecological‐constraints model predicts that within‐group feeding competition will increase as group size increases, necessitating more daily travel to find food and thereby constraining group size. It provides a useful tool for detecting scramble competition any time it is difficult to determine whether or not food is limiting. We tested the ecological‐constraints model on highly folivorous ursine colobus monkeys (Colobus vellerosus) at the Boabeng‐Fiema Monkey Sanctuary in Ghana. Three differently sized groups were followed for 13 months and two others were followed for 6 months each in 2004–2005 using focal‐animal sampling and ranging scans; ecological plots and phenology surveys were used to determine home‐range quality and food availability. There was relatively little difference in home‐range quality, monthly food availability, diet, adult female ingestion rates, and rate of travel within food patches between the groups. However, home‐range size, day‐range length, and percent of time spent feeding all increased with group size. We performed a single large test of the ecological‐constraints model by combining several separate Spearman correlations, each testing different predictions under the model, using Fishers log‐likelihood method. It showed that the ecological‐constraints model was supported in this study; scramble competition in this population is manifesting in increased ranging and time spent feeding. How costly this increased energy expenditure is for individuals in larger groups remains to be determined. Am. J. Primatol. 71:49–59, 2009.

Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng‐Fiema, Ghana: Possible anthropozoonotic transmission

Parasite richness and prevalence in wild animals can be used as indicators of population and ecosystem health. In this study, the gastrointestinal parasites of ursine colobus monkeys (Colobus vellerosus) at the Boabeng-Fiema Monkey Sanctuary (BFMS), Ghana, were investigated. BFMS is a sacred grove where monkeys and humans have long lived in relatively peaceful proximity. Fecal samples (n = 109) were collected opportunistically from >27 adult and subadult males in six bisexual groups and one all-male band from July 2004 to August 2005. Using fecal floatation, we detected three protozoans (two Entamoeba sp., Isospora sp.), five nematodes (Ascaris sp., Enterobius sp., Trichuris sp., two strongyle sp.), and one digenean trematode. Using fluorescein labeled antibodies, we detected an additional protozoan (Giardia sp.), and with PCR techniques, we characterized this as G. duodenalis Assemblage B and also identified a protistan (Blastocystis sp., subtype 2). The most prevalent parasite species were G. duodenalis and Trichuris sp. Parasites were more prevalent in the long wet season than the long dry. Parasite prevalence did not vary by age, and average parasite richness did not differ by rank for males whose status remained unchanged. However, males that changed rank tended to show higher average parasite richness when they were lower ranked. Individuals that spent more time near human settlements had a higher prevalence of Isospora sp. that morphologically resembled the human species I. belli. The presence of this parasite and G. duodenalis Assemblage B indicates possible anthropozoonotic and/or zoonotic transmission between humans and colobus monkeys at this site.

Dispersal in male ursine colobus monkeys (Colobus vellerosus): influence of age, rank and contact with other groups on dispersal decisions

[Dispersal is male-biased in ursine colobus monkeys ( Colobus vellerosus ), although female dispersal also occurs (Teichroeb et al., 2009). Here we describe the process of male dispersal and its connection with between-group encounters (BGEs, N = 444) and male incursions (when males left their group and approached within 50 m of another group; N = 128) at the Boabeng-Fiema Monkey Sanctuary in central Ghana. Through BGEs and incursions, particularly those with non-aggressive interactions between individuals in different groups (BGEs, N = 17; incursions, N = 4), males could probably assess other groups for dispersal opportunities. There was a trend for males to perform incursions more frequently before emigrating voluntarily than involuntarily. Incursions were often performed towards the group that the male eventually transferred to. Incursions by alpha males were temporally shorter and more aggressive than those by non-alpha males. We suggest that non-alpha males used incursions to assess other groups for breeding or dispersal opportunities, whereas alpha males performed incursions mainly to convey information about their quality to neighbouring males and females. Male emigrations/disappearances (natal N = 20, secondary N = 43, unknown N = 9) and immigrations ( N = 62) were recorded for seven groups during ten years (2000– 2010). Alpha males always emigrated involuntarily. Parallel emigration and immigration occurred. Males often immigrated into groups with a more favourable adult male/adult female ratio and improved their rank, both of which likely increased their mating opportunities. The most fitting ultimate explanation for both natal and secondary male dispersal in this population was the intrasexual competition for mates hypothesis, as males of all ages appeared to emigrate to improve their reproductive opportunities., Dispersal is male-biased in ursine colobus monkeys (Colobus vellerosus), although female dispersal also occurs (Teichroeb et al., 2009). Here we describe the process of male dispersal and its connection with between-group encounters (BGEs, N = 444) and male incursions (when males left their group and approached within 50 m of another group; N = 128) at the Boabeng-Fiema Monkey Sanctuary in central Ghana. Through BGEs and incursions, particularly those with non-aggressive interactions between individuals in different groups (BGEs, N = 17; incursions, N = 4), males could probably assess other groups for dispersal opportunities. There was a trend for males to perform incursions more frequently before emigrating voluntarily than involuntarily. Incursions were often performed towards the group that the male eventually transferred to. Incursions by alpha males were temporally shorter and more aggressive than those by non-alpha males. We suggest that non-alpha males used incursions to assess other groups for breeding or dispersal opportunities, whereas alpha males performed incursions mainly to convey information about their quality to neighbouring males and females. Male emigrations/disappearances (natal N = 20, secondary N = 43, unknown N = 9) and immigrations (N = 62) were recorded for seven groups during ten years (2000– 2010). Alpha males always emigrated involuntarily. Parallel emigration and immigration occurred. Males often immigrated into groups with a more favourable adult male/adult female ratio and improved their rank, both of which likely increased their mating opportunities. The most fitting ultimate explanation for both natal and secondary male dispersal in this population was the intrasexual competition for mates hypothesis, as males of all ages appeared to emigrate to improve their reproductive opportunities.]

Comparison of habitat quality and diet of Colobus vellerosus in forest fragments in Ghana

The forest fragments surrounding the Boabeng-Fiema Monkey Sanctuary (BFMS) in central Ghana shelter small populations of Colobus vellerosus. Little is known about these populations or the ability of the fragments to support them, despite the fact that these fragments represent potentially important habitat for the colobus in this region. We compared the diet of three groups of C. vellerosus in the fragments to two groups in BFMS. We also examined the differences in plant species composition and food abundance among fragments. The study took place from June to November 2003. Dietary data were collected using scan sampling. Plant species composition and food abundance were evaluated using tree plots and large tree surveys. As in BFMS groups, leaves constituted the highest proportion of the diet of fragment groups, yet the colobus in fragments fed on more lianas than did those in BFMS. Over 50% of all species observed eaten by colobus in the fragments were not consumed in BFMS groups during the same season. Food abundance was similar between fragments and BFMS, although species composition differed. There was no relationship between the density of colobus and the density of food trees or percentage of food species, suggesting that other factors may be influencing the number of colobus present. This study highlights the broad dietary range of C. vellerosus, which may be a factor allowing its survival in these fragments.

Reproductive monitoring of free-ranging female mountain gorillas by urinary hormone analysis.

Frequent urine samples from three habituated free‐ranging adult female mountain gorillas were collected during a four‐week period in order to characterize, by analysis of urinary hormones, their ovarian cycle, and to diagnose pregnancy. A conceptive cycle and two cycles that did not result in full term pregnancy were monitored. Behavioral and physiological observations of mating and labial swellings were correlated to urinary hormone results. Mating occurred on days with elevated estrogens. Labial swelling was maximum near or at peak estrogen levels. Pregnancy was diagnosed at the field site by measurement of chorionic gonadotropin using commercially available human pregnancy detection kits. In one pregnancy, gestation length was 254 days. The pregnanediol glucuronide concentrations of the mountain gorilla did not change during the nonconceptive cycle. During the conceptive cycle, the concentrations did not increase until the approximate time of implantation. This finding suggests marked differences in steroid production or metabolism between the mountain gorilla and the captive lowland gorilla. Am. J. Primatol. 51:209–215, 2000.

Activity Budget and Ranging Patterns of Colobus vellerosus in Forest Fragments in Central Ghana

The forest fragments surrounding the 192-ha Boabeng-Fiema Monkey Sanctuary (BFMS) in central Ghana contain small populations of Colobus vellerosus. Data were collected on activity budget, ranging patterns and habitat use of 3 groups living in these small fragments in August–November 2003, and compared to 3 BFMS groups. Fragment groups spent less time moving and more time resting than BFMS groups. Home ranges of fragment groups tended to be smaller than those of BFMS groups. Fragment and BFMS groups used similarly sized trees. Comparisons of activity budget and ranging between fragments and the BFMS suggest that fragment habitat quality was sufficient to sustain current numbers. These behavioral trends are consistent with a concurrent study that we conducted investigating ecological quality in the same fragments.