Julie A. Teichroeb

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.]

Cost-free vigilance during feeding in folivorous primates? Examining the effect of predation risk, scramble competition, and infanticide threat on vigilance in ursine colobus monkeys (Colobus vellerosus)

Vigilance often decreases with increasing group size, due to lower predation risk or greater scramble competition for food. A group size effect on vigilance is seldom seen in primates, perhaps because scanning and feeding often occur simultaneously or because the distinction between routine and induced vigilance has not been investigated. We analyzed feeding and resting observations separately while distinguishing between routine and induced scans in four groups of wild ursine colobus monkeys (Colobus vellerosus) experiencing scramble competition for food and infanticide risk. We used linear mixed-effect models to test the effect of group size, age–sex class, number of neighbors, number of adult male neighbors, and height in the canopy on scanning rates (vigilance) with and without evident conspecific threat. Food type was also examined in the feeding models. Perceived predation risk affected vigilance more than scramble competition for food and infanticide risk. Routine and induced vigilance were greatest at lower canopy heights during feeding and resting and increased when individuals had fewer neighbors while resting. A group size effect was found on induced vigilance while resting, but scanning increased with group size, which probably indicates visual monitoring of conspecifics. Scanning rates decreased while feeding on foods that required extensive manipulation. This supports the idea that vigilance is relatively cost free for upright feeders when eating food that requires little manipulation, a common feature of folivore diets. In the presence of threatening conspecific males, close proximity to resident males decreased individual vigilance, demonstrating the defensive role of these males in the group.

Aspects of Male Competition in Colobus vellerosus: Preliminary Data on Male and Female Loud Calling, and Infant Deaths After a Takeover

Male Colobus vellerosus are the main participants in intergroup encounters, and lead incursions in neighboring groups during which they attack infants. Extragroup copulations, all-male groups, and male takeover occur in the species. Here, we provide additional information on behaviors associated with male reproductive competition in Colobus vellerosus. We examined 1 resident male loud calling and participation in intergroup encounters in relation to a takeover. We also report a second case of takeover that led to the death of the former resident male and the death of 2 male infants, presumably as a result of aggression from the all-male group. The new resident male wounded the third infant of the group, which apparently died after its mother abandoned it. During the period characterized by the attacks on the infant and after its disappearance, females initiated and participated in loud call bouts with the new resident male. We examine the possible functions of female loud calling, and suggest that in this context, it might force the resident male to call along to indicate his presence.

Individualistic female dominance hierarchies with varying strength in a highly folivorous population of black-and-white colobus

Females that do not experience strong contest competition for food are presumed to form ‘egalitarian’ relationships (i.e., lacking strong, linear dominance hierarchies). However, recent studies of Gorilla beringei beringei (mountain gorilla) have documented relatively strong, linear female dominance hierarchies despite them having a highly folivorous diet that generates relatively low levels of within-group contest competition (Robbins et al., 2005, 2007). To investigate if this pattern holds true for other highly folivorous species that may experience low levels of contest competition, we examined the linearity and strength of female dominance hierarchies in a population of Colobus vellerosus (ursine colobus or white-thighed colobus) at Boabeng-Fiema, Ghana. From 2004 to 2011, we collected data via ad libitum and focal sampling of 75 adult and subadult females in eight groups. Half of the study groups had few unknown submissive relationships, and females formed individualistic hierarchies with high linearity indices ranging from 0.9 to 1. There was between-group variation in all components of hierarchical strength (i.e., hierarchical expression, consistency, and stability). Groups showed varying rates of submission, and there was a short latency to detect a linear hierarchy in some groups and a long latency in other groups (i.e., varying levels of hierarchical expression). Females in most groups formed unidirectional and stable relationships. Maturing females challenged older females in some groups, and these groups had more non-linear relationships (i.e., dyads with more submissive interactions down rather than up the hierarchy) and higher rates of individual rank change than other groups. Based on low rates of submission, long latencies, and/or some inconsistencies, we conclude that most groups form relatively

Distribution of diurnal primate species in Togo and Bénin.

The Dahomey Gap, a strip of forest-savanna mosaic that interrupts the lowland rainforests of West Africa, is supposed to have acted as a natural barrier to the distribution of forest-dwelling mammals. However, few thorough mammal surveys have been conducted in this region. This study intended to gather distributional data and help clarify the distribution limits of diurnal primates occurring within this ‘Gap’. Southern Togo and Bénin were surveyed between June and November 2003. The surveys consisted of interviews with hunters and guards from parks and reserves, and walking surveys of forests. As a result, seven diurnal primate species are listed for Togo and Bénin.

Alpha male replacements in nonhuman primates: Variability in processes, outcomes, and terminology

Alpha male replacements occur in all primates displaying a dominance hierarchy but the process can be extremely variable. Here, we review the primate literature to document differences in patterns of alpha male replacements, showing that group composition and dispersal patterns account for a large proportion of this variability. We also examine the consequences of alpha male replacements in terms of sexual selection theory, infanticide, and group compositions. Though alpha male replacements are often called takeovers in the literature, this term masks much of the variation that is present in these processes. We argue for more concise terminology and provide a list of terms that we suggest more accurately define these events. Finally, we introduce the papers in this special issue on alpha male replacements in the American Journal of Primatology and discuss areas where data are still lacking.