Peter J. Fashing

Male and female strategies during intergroup encounters in guerezas (Colobus guereza): evidence for resource defense mediated through males and a comparison with other primates

Abstract. Although socioecological theory predicts that differences in male and female parental investment will be reflected in their behavior during intergroup encounters, the strategies actually pursued by adults of each sex during intergroup encounters remain poorly known for most primate species. Over an 11-month period, I examined the functions of adult male and female participation in intergroup aggression in five groups of eastern black-and-white colobus monkeys, or guerezas (Colobus guereza), in the Kakamega Forest, Kenya. Guerezas are large-bodied arboreal African colobine monkeys that usually live in one-male multifemale groups, though multimale multifemale groups are not uncommon. During 174 study days, I observed 136 encounters, most of which were aggressive in nature. I evaluated the hypotheses that through intergroup aggression (1) males were directly defending mates, (2) males were indirectly defending mates by directly defending food resources, (3) males were attempting to attract mates via infanticide, and/or (4) females were defending food resources. I found strong evidence consistent with both the direct male mate defense and indirect male mate defense via resource defense hypotheses, but no evidence consistent with the male mate attraction via infanticide hypothesis. There was little evidence in favor of the female resource defense hypothesis beyond the fact that females occasionally participated in intergroup aggression in four of the five study groups. A review of the most intensive studies of primate intergroup encounters suggests that direct male mate defense may occur in almost all primate species, while female resource defense appears to be most common in species with high levels of female philopatry. The indirect male mate defense via resource defense strategy has rarely been evaluated and may be a more common male strategy than is currently believed. I present a hypothesis that predicts when male primates are expected to defend resources for females in their group.

Diurnal primate densities and biomass in the Kakamega Forest: an evaluation of census methods and a comparison with other forests.

Line‐transect surveys were conducted at the Isecheno study site in the Kakamega Forest, western Kenya to estimate diurnal primate densities. The estimates from several different methods of analysis of census data were compared to “true” density values based on home range size and overlap for two species. The Whitesides method [Whitesides et al., 1988], which incorporates species‐specific mean group spread into its formula for estimating transect width, provided the most accurate density estimates. The importance of including as many groups as possible when calculating density from home range size and overlap is demonstrated with long‐term data from Colobus guereza and Cercopithecus mitis. Colobus guereza group density at Isecheno was much lower than that published from a recent brief study [von Hippel, 1996]. Cercopithecus mitis group density has fallen while overall population biomass appears to have remained stable over 20 years of study. Isecheno has the second highest diurnal primate biomass of the ten Guineo‐Congolian rainforest sites for which biomass data are available, despite having the lowest primate species richness. Within the Guineo‐Congolian rainforest system, primate biomass appears to vary to some extent between ecogeographic regions: two of three mid‐elevation East African sites have high biomasses, two of two lowland West African sites have intermediate biomasses, and four of five lowland Central African sites have low biomasses. There is a strong positive correlation between total colobine biomass and total primate biomass at the ten Guineo‐Congolian rainforest sites. Am. J. Primatol. 50:139–152, 2000.

Activity and Ranging Patterns of Guerezas in the Kakamega Forest: Intergroup Variation and Implications for Intragroup Feeding Competition

From March 1997 to February 1998, I investigated the activity patterns of 2 groups and the ranging patterns of 5 groups of eastern black-and-white colobus (Colobus guereza), aka guerezas, in the Kakamega Forest, Kenya. Guerezas at Kakamega spent more of their time resting than any other population of colobine monkeys studied to date. In addition, I recorded not one instance of intragroup aggression in 16,710 activity scan samples, providing preliminary evidence that intragroup contest competition may be rare or absent among guerezas at Kakamega. Mean daily path lengths ranged from 450 to 734 m, and home range area ranged from 12 to 20 ha, though home range area may have been underestimated for several of the study groups. Home range overlap was extensive with 49–83% of each groups range overlapped by the ranges of other groups. Despite the high level of home range overlap, the frequently entered areas (quadrats entered on ≥30% of a groups total study days) of any one group were not frequently entered by any other study group. Mean daily path length is not significantly correlated with levels of availability or consumption of any plant part item. Mean daily path length is also not significantly correlated with group size, though the largest group did have the longest mean daily path length. This finding suggests that intragroup scramble competition may have been rare or absent among guerezas at Kakamega except perhaps in the largest group, which was unusually large.

Long-term tree population dynamics and their implications for the conservation of the Kakamega Forest, Kenya

Long-term studies of tree population dynamics play an important role in identifying the conservation needs of tropical forest ecosystems. We examined changes in tree population structure and composition over an 18-year period (1981–1999) in three plots located at the center of the Isecheno study site in the Kakamega Forest, Kenya, a forest with a history of logging and other anthropogenic disturbance. DBH size class distribution took the shape of an ‘inverse J’ curve in both 1981 and 1999 and did not differ significantly between the two study periods. Stem density increased significantly during the study with most of the increase occurring in the smallest stem size class (10–14 cm DBH). Nearly all of the most common species in 1981 remained among the most common in 1999, though the density of pioneer species decreased by 21% during the study. Our results suggest that forest in the study plots remained relatively undisturbed and in good condition over the study period. Forest in the plots also appeared still to be recovering from the selective logging of large trees that took place at Isecheno in the 1940s. In addition to our longitudinal study, we compared tree population parameters at three additional Isecheno sites spread over a distance of ∼1 km that have experienced different histories of disturbance: (i) a lightly human disturbed site (LHD), (ii) a heavily human disturbed site (HHD), and (iii) a cattle disturbed site (CD). While all three sites were selectively logged in the 1940s, the main signs of disturbance today are footpaths at the LHD site, tree stumps at the HHD site, and wide cattle paths at the CD site. Not surprisingly, of the disturbed sites, the LHD site was in the best condition. Trees at the HHD site exhibited extremely poor recruitment into the small size classes, a condition that can probably be attributed to human exploitation of small trees for poles. The CD site appeared to be at an earlier successional stage than the other disturbed sites with its low mean DBH, high overall stem density, and high pioneer species stem density. Browsing and trampling of vegetation by cattle may be the source of the light gaps that have led to the abundance of pioneer species at this site. We conclude that conservation measures applied to central Isecheno, including the establishment of a forest station nearby and ranger patrols, appear to have succeeded, but that the prognosis for the Kakamega Forest in general is bleak if protection efforts are not increased in other parts of the forest, where anthropogenic disturbance remains high. We also note the considerable variation in tree population structure and composition that can occur within a small area depending on the local history of disturbance.

Feeding Ecology of Guerezas in the Kakamega Forest, Kenya: The Importance of Moraceae Fruit in Their Diet

Eastern black-and-white colobus (Colobus guereza), or guerezas, have long been considered to be one of the most folivorous primates. I conducted a study of the feeding ecology of two guereza groups (T and O) over an annual cycle in the Kakamega Forest of western Kenya. I found that the annual diets of both groups comprised mostly of leaves (T: 48%, O: 57%) though fruit (T: 44%, O: 33%) also accounted for a substantial portion of the diet. In the six months when fruit was most abundant, fruit consumption constituted an average of 58% of T-groups monthly diet and 42% of O-groups monthly diet. In contrast to most previous studies of colobines, in which seeds were the primary fruit item consumed, almost all of the fruit eaten by guerezas at Kakamega consisted of whole fruits. At least 72% of the whole fruits consumed by T-and O-groups were whole fruits from trees in the Moraceae family, which dominates the tree family biomass at Kakamega. Unlike at sites where guerezas consumed fruit primarily when young leaves were scarce, at Kakamega guerezas ate fruit in accordance with its availability and irrespective of the availability of young leaves. My findings demonstrate that guerezas are more dietarily flexible than was previously known, which may help to explain why the species can survive in such a wide variety of forested habitats across equatorial Africa.

Spatial Patterning in Nocturnal Prosimians: A Review of Methods and Relevance to Studies of Sociality

Patterns of home range overlap between individuals are key parameters used in discussions of sociality in nocturnal prosimians. Despite the importance of space use variables in defining social structure in nocturnal prosimians, researchers have yet to reach a consensus concerning the most reliable techniques for measuring patterns of home range use. In this paper, we review the methods used in 27 studies of nocturnal prosimian ranging behavior published since 1977. We discuss the usefulness and limitations of the various methods of data collection (radio tracking, trap mark, and identification of sleeping site locations) and data analysis (minimum convex polygon method, minimum concave polygon method, and quadrat analysis) used in these studies. We conclude that the most effective method for gathering data on individual movements and social interactions is direct observation of individual radio tagged animals during all‐night follows. In those cases where radio tracking and/or all‐night follows are not possible, trap mark techniques can be used, although they tend to greatly underestimate home range size. We recommend that data collected on nocturnal prosimian ranging behavior be analyzed using the minimum convex polygon method, quadrat analysis, and, perhaps, one other of the more mathematically sophisticated techniques popular in studies of non‐primate mammals. Finally, we urge researchers to employ standardized methods of data collection and data analysis in future studies of range use in nocturnal prosimians. Without standardization of methods, quantitative comparisons of the findings from different studies are biologically meaningless and prevent cross‐species comparisons of space use and its relation to sociality. Am. J. Primatol. 51:3–19, 2000.

Effects of dietary fracture toughness and dental wear on chewing efficiency in geladas (Theropithecus gelada)

Chewing efficiency has been associated with fitness in mammals, yet little is known about the behavioral, ecological, and morphological factors that influence chewing efficiency in wild animals. Although research has established that dental wear and food material properties independently affect chewing efficiency, few studies have addressed the interaction among these factors. We examined chewing efficiency, measured as mean fecal particle size, as a function of seasonal shifts in diet (and corresponding changes in food fracture toughness) in a single breeding population of a grazing primate, the gelada monkey, at Guassa, Ethiopia. We also measured dental topographic traits (slope, angularity, and relief index) and relative two- and three-dimensional shearing crest lengths in a cross-sectional wear series of gelada molars. Chewing efficiency decreased during the dry season, a pattern corresponding to the consumption of foods with higher fracture toughness. Older individuals experienced the most pronounced decreases in chewing efficiency between seasons, implicating dental wear as a causal factor. This pattern is consistent with our finding that dental topographic metrics and three-dimensional relative shearing crest lengths were lowest at the last stage of wear. Integrating these lines of behavioral, ecological, and morphological evidence provides some of the first empirical support for the hypothesis that food fracture toughness and dental wear together contribute to chewing efficiency. Geladas have the highest chewing efficiencies measured thus far in primates, and may be analogous to equids in their emphasis on dental design as a means of particle size reduction in the absence of highly specialized digestive physiology.

Death among geladas (Theropithecus gelada): a broader perspective on mummified infants and primate thanatology.

Despite intensive study in humans, responses to dying and death have been a neglected area of research in other social mammals, including nonhuman primates. Two recent reports [Anderson JR, Gillies A, Lock LC. 2010. Pan thanatology. Current Biology 20:R349–R351; Biro D, Humle T, Koops K, Souse C, Hayashi M, Matsuzawa T. 2010. Chimpanzee mothers at Bossou, Guinea carry the mummified remains of their dead infants. Current Biology 20:R351–R352] offered exciting new insights into behavior toward dying and dead conspecifics in our closest living relatives—chimpanzees. Here, we provide a comparative perspective on primate thanatology using observations from a more distant human relative—gelada monkeys (Theropithecus gelada)—and discuss how gelada reactions to dead and dying groupmates differ from those recently reported for chimpanzees. Over a 3.75‐year study period, we observed 14 female geladas at Guassa, Ethiopia carrying dead infants from 1 hr to ≥48 days after death. Dead infants were carried by their mothers, other females in their group, and even by females belonging to other groups. Like other primate populations in which extended (>10 days) infant carrying after death has been reported, geladas at Guassa experience an extreme climate for primates, creating conditions which may favor slower rates of decomposition of dead individuals. We also witnessed the events leading up to the deaths of two individuals and the responses by groupmates to these dying individuals. Our results suggest that while chimpanzee mothers are not unique among primates in carrying their dead infants for long periods, seemingly “compassionate” caretaking behavior toward dying groupmates may be unique to chimpanzees among nonhuman primates (though it remains unknown whether such “compassionate” behavior occurs outside captivity). Am. J. Primatol. 73:405–409, 2011.

Newly discovered Bale monkey populations in forest fragments in southern Ethiopia: evidence of crop raiding, hybridization with grivets, and other conservation threats.

Until recently, the Bale monkey (Chlorocebus djamdjamensis), an arboreal primate endemic to the southern Ethiopian highlands, remained virtually unstudied, and its distribution pattern inadequately documented. To broaden our knowledge of the species’ distribution and abundance, we carried out interviews with local people and total count surveys for Bale monkeys across 67 fragmented forest sites in human‐dominated landscapes in the Oromia and Southern Nations, Nationalities, and Peoples Regions, Ethiopia. From January 2010 to May 2011, we discovered 26 new Bale monkey populations inhabiting forest fragments at elevations ranging from 2,355 to 3,204 m asl. Across these populations, we recorded 37 groups ranging in size from 9 to 29 individuals (Mean = 19.5, SD = 4.5), for a total of 722 individuals. Black‐and‐white colobus monkeys (Colobus guereza) were sympatric with Bale monkeys at all sites, while grivet monkeys (Chlorocebus aethiops) were found only at sites where Bale monkeys did not occur. All of the newly discovered Bale monkey sites once contained bamboo forest, though at 35% of the sites bamboo forest had been eliminated during the past two decades. The persistence of Bale monkeys at fragmented sites lacking bamboo suggests greater habitat flexibility for the species than previously thought, though the long‐term viability of populations both with and without bamboo remains uncertain. Human hunting in response to crop raiding, a behavior the monkeys engaged in at all sites, represents a major threat facing the newly discovered Bale monkey populations. Furthermore, despite their current lack of sympatry, apparently hybrid individuals between Bale monkeys and grivets were noted at three sites, posing yet another potential obstacle to Bale monkey conservation. Community conservation programs aimed at (1) protecting remaining habitat fragments, (2) planting bamboo and trees within and between fragments, and (3) reducing crop raiding represent the only hope for survival of the newly discovered Bale monkey populations. Am. J. Primatol. 74:423‐432, 2012.

Evaluating the suitability of planted forests for African forest monkeys: a case study from Kakamega forest, Kenya

As natural forest cover declines, planted forests have come to occupy an increasing percentage of the earths surface, yet we know little about their suitability as alternative habitat for wildlife. Although some primate species use planted forests, few studies have compared primate populations in natural and nearby planted forests. From March 2006 to July 2010, we conducted line transect surveys and assessed group sizes and compositions in natural and nearby 60–70 year old mixed indigenous planted forest to determine the densities of diurnal primate species (Colobus guereza, Cercopithecus mitis, C. ascanius) in these two forest types at Isecheno, Kakamega Forest, Kenya. Line transect data were analyzed using the Encounter Rate, Whitesides, and Distance sampling methods, which all provided broadly consistent results. We found that all three diurnal primate species occupy both natural and planted forest at Isecheno. However, group densities of the two Cercopithecus species were 42–46% lower in planted than in natural forest. Colobus guereza achieved comparable group densities in the two forest types, although the species is found in smaller groups, and thus at lower (35%) individual density, in planted than in natural forest. Following a logging episode in the planted forest mid‐way through our study, Cercopithecus ascanius group densities fell by 60% while C. mitis and Colobus guereza group densities remained stable over the next two years. Overall, our results suggest that while primate species vary in their response to habitat disturbance, planted forest has the potential to contribute to the conservation of some African monkey species. Even for the relatively flexible taxa in our study, however, 60–70 year old mixed indigenous planted forest failed to support densities comparable to those in nearby natural forest. From the perspective of Kakamegas primates, planted forests may supplement natural forest, but are not an adequate replacement for it. Am. J. Primatol. 73:1–14, 2011.