Lynne A. Isbell

Demography and Life Histories of Sympatric Patas Monkeys, Erythrocebus patas, and Vervets, Cercopithecus aethiops, in Laikipia, Kenya

Mortality patterns are thought to be strong selective forces on life history traits, with high adult mortality and low immature mortality favoring early and rapid reproduction. Patas monkeys (Erythrocebus patas) have the highest potential rates of population increase for their body size of any haplorhine primate because they reproduce both earlier and more often. We report here 10xa0yr of comparative demographic data on a population of patas monkeys and a sympatric population of vervet monkeys (Cercopithecus aethiops), a closely related species differing in aspects of social system, ecology, and life history. The data reveal that 1) adult female patas monkeys have significantly higher mortality than adult female vervets; 2) infant mortality in patas monkeys is relatively low compared to the norm for mammals because it is not significantly different from that of adult female patas monkeys; and 3) infant mortality is significantly higher than adult female mortality in vervets. For both species, much of the mortality could be attributed to predation. An epidemic illness was also a major contributor to the mortality of adult female patas monkeys whereas chronic exposure to pathogens in a cold and damp microenvironment may have contributed to the mortality of infant vervets. Both populations experienced large fluctuations during the study period. Our results support the prediction from demographic models of life history evolution that high adult mortality relative to immature mortality selects for early maturation.

Food site residence time and female competitive relationships in wild gray-cheeked mangabeys (Lophocebus albigena)

Authors of socioecological models propose that food distribution affects female social relationships in that clumped food resources, such as fruit, result in strong dominance hierarchies and favor coalition formation with female relatives. A number of Old World monkey species have been used to test predictions of the socioecological models. However, arboreal forest-living Old World monkeys have been understudied in this regard, and it is legitimate to ask whether predominantly arboreal primates living in tropical forests exhibit similar or different patterns of behavior. Therefore, the goal of our study was to investigate female dominance relationships in relation to food in gray-cheeked mangabeys (Lophocebus albigena). Since gray-cheeked mangabeys are largely frugivorous, we predicted that females would have linear dominance hierarchies and form coalitions. In addition, recent studies suggest that long food site residence time is another important factor in eliciting competitive interactions. Therefore, we also predicted that when foods had long site residence times, higher-ranking females would be able to spend longer at the resource than lower-ranking females. Analyses showed that coalitions were rare relative to some other Old World primate species, but females had linear dominance hierarchies. We found that, contrary to expectation, fruit was not associated with more agonism and did not involve long site residence times. However, bark, a food with a long site residence time and potentially high resource value, was associated with more agonism, and higher-ranking females were able to spend more time feeding on it than lower-ranking females. These results suggest that higher-ranking females may benefit from higher food and energy intake rates when food site residence times are long. These findings also add to accumulating evidence that food site residence time is a behavioral contributor to female dominance hierarchies in group-living species.

Microhabitat Preference and Vertical Use of Space by Patas Monkeys (Erythrocebus patas) in Relation to Predation Risk and Habitat Structure

Habitat structure can be important in determining habitat preference of animals because it is often closely linked to factors that affect survival and reproduction, such as food availability and predation risk. Here we examine the ways in which microhabitat structure and predation risk affect the habitat preference of wild patas monkeys (Erythrocebus patas). Patas monkeys in Kenya are typically restricted to Acacia drepanolobium habitat, but within our study group’s home range, there are two distinct microhabitats, one with taller trees (‘tall microhabitat’) and one with apparently perennially shorter trees (‘short microhabitat’). Examination of ranging behavior indicates that the patas monkeys preferred the tall microhabitat. In the tall microhabitat, focal animals climbed into trees that were significantly taller than average, indicating that they preferred tall trees. Female patas monkeys spent more time scanning from tall trees than from short trees and detected predators only from taller than average trees, based on alarm call data. Their use of tall trees may have decreased their predation risk by increasing their ability to detect predators. We found no evidence of increased food availability or reduced predator presence in the tall microhabitat that could contribute to the monkeys’ preference for the tall microhabitat.

Male Demography, Female Mating Behavior, and Infanticide in Wild Patas Monkeys (Erythrocebus patas)

Infanticide by males has been hypothesized to be a naturally selected behavioral strategy that increases the infanticidal males reproductive success. The sexual selection hypothesis has been challenged via alternative, nonadaptive hypotheses that dispute its empirical and theoretical bases. Two of the most widely recognized alternatives are the social pathology hypothesis, in which infanticide results from overcrowding or recent human disturbance, and the generalized aggression hypothesis, in which infanticide is an epiphenomenon of increased male aggression. We report the first case of infanticide in wild, seasonally breeding patas monkeys (Erythrocebus patas) living at a low population density in a stable habitat, conditions which do not support the social pathology hypothesis. Its exceptional occurrence is consistent with the sexual selection hypothesis: over a 7-year period the infanticidal male was the only one of 13 resident males that was not present during the actual conception season but was present during the following birth season. Also consistent with this hypothesis, mothers were differentially targeted for male aggression, which increased sevenfold during the days surrounding the infanticide and then decreased to baseline levels after the infanticide. Aggression targeted at mothers does not support the generalized aggression hypothesis. As predicted by the sexual selection hypothesis, females began soliciting mating immediately after the infanticide, despite its occurrence in the nonconceptive season.

After the fire: benefits of reduced ground cover for vervet monkeys (Cercopithecus aethiops)

Here we describe changes in ranging behavior and other activities of vervet monkeys (Cercopithecus aethiops) after a wildfire eliminated grass cover in a large area near the study groups home range. Soon after the fire, the vervets ranged farther away from tall trees that provide refuge from mammalian predators, and moved into the burned area where they had never been observed to go before the fire occurred. Visibility at vervet eye‐level was 10 times farther in the burned area than in unburned areas. They traveled faster, and adult females spent more time feeding and less time scanning bipedally in the burned area than in the unburned area. The burned areas greater visibility may have lowered the animals perceived risk of predation there, and may have provided them with an unusual opportunity to eat acacia ants. Am. J. Primatol. 71:252–260, 2009.

Color Vision Variation and Foraging Behavior in Wild Neotropical Titi Monkeys (Callicebus brunneus): Possible Mediating Roles for Spatial Memory and Reproductive Status

The selective advantages to primates of trichromatic color vision, allowing discrimination among the colors green, yellow, orange, and red, remain poorly understood. We test the hypothesis that, for primates, an advantage of trichromacy over dichromacy, in which such colors are apt to be confused, lies in the detection of yellow, orange, or red (YOR) food patches at a distance, while controlling for the potentially confounding influences of reproductive status and memory of food patch locations. We employ socially monogamous titi monkeys (Callicebus brunneus) which, like most platyrrhine primates, have polymorphic color vision resulting in populations containing both dichromatic and trichromatic individuals. Wild Callicebus brunneus spent most foraging time in YOR food patches, the locations of most of which were likely to have been memorable for the subjects. Overall, both dichromatic and trichromatic females had significantly higher encounter rates than their dichromatic male pair mates for low-yield ephemeral YOR food patches whose locations were less likely to have been remembered. We detected no difference in the encounter rates of dichromatic and trichromatic females for such patches. However, the data suggest that such a difference may be detectable with a larger sample of groups of Callicebus brunneus, a larger sample of foraging observations per group, or both. We propose that a trichromatic advantage for foraging primates may be realized only when individuals’ energy requirements warrant searching for nonmemorable YOR food patches, a context for selection considerably more limited than is often assumed in explanations of the evolution of primate color vision.

Scales drive detection, attention, and memory of snakes in wild vervet monkeys (Chlorocebus pygerythrus)

Predatory snakes are argued to have been largely responsible for the origin of primates via selection favoring expansion of the primate visual system, and even today snakes can be deadly to primates. Neurobiological research is now beginning to reveal the mechanisms underlying the ability of primates (including humans) to detect snakes more rapidly than other stimuli. However, the visual cues allowing rapid detection of snakes, and the cognitive and ecological conditions contributing to faster detection, are unclear. Since snakes are often partially obscured by vegetation, the more salient cues are predicted to occur in small units. Here we tested for the salience of snake scales as the smallest of potential visual cues by presenting four groups of wild vervet monkeys (Chlorocebus pytherythrus) with a gopher snake (Pituophis catenifer) skin occluded except for no more than 2.7xa0cm, in natural form and flat, the latter to control for even small curvilinear cues from their unusual body shape. Each of these treatments was preceded by a treatment without the snakeskin, the first to provide a baseline, and the second, to test for vigilance and memory recall after exposure to the snakeskin. We found that (1) vervets needed only a small portion of snakeskin for detection, (2) snake scales alone were sufficient for detection, (3) latency to detect the snakeskin was longer with more extensive and complex ground cover, and (4) vervets that were exposed to the snakeskin remembered where they last saw “snakes”, as indicated by increased wariness near the occluding landmarks in the absence of the snakeskin and more rapid detection of the next presented snakeskin. Unexpectedly, adult males did not detect the snakeskin as well as adult females and juveniles. These findings extend our knowledge of the complex ecological and evolutionary relationships between snakes and primates.

Why Vervet Monkeys (Cercopithecus aethiops) Live in Multimale Groups

Explanations of patterns of male residence in primate groups have long been sought by behavioral ecologists. The permanent co-existence of multiple males with groups of females is unusual in mammals, but primates include a large number of such species. In cercopithecine primates alone, 17 of 44 species (39%) live in multimale groups year-round (Smuts et al., 1987). Suggested determinants of male residence patterns in primates include phylogenetic constraints (Struhsaker, 1969), female defensibility (numbers of females, or temporal and spatial distribution of females) (Clutton-Brock and Harvey, 1977; Wrangham, 1979, 1980; van Schaik and van Hooff, 1983; Terborgh, 1983; Andelman, 1986; Ridley, 1986; Dunbar, 1988; Altmann, 1990; Janson, 1992; Mitani et al., 1996; Nunn, 1999), predation (Struhsaker, 1969; Crook, 1972; Henzi, 1988; van Schaik and van Noordwijk, 1989;

Changes in ranging and agonistic behavior of vervet monkeys (Cercopithecus aethiops) after predator-induced group fusion

Socio‐ecological theory predicts that group fusion in female‐philopatric primate species will be rare because females experience increased costs by associating with non‐relatives. Indeed, fusion has been reported only 14 times in only 4 female‐philopatric cercopithecines despite many years of observation. Here, we describe changes in ranging and agonistic behavior of vervet monkeys (Cercopithecus aethiops) after the fusion of two groups, the sole group fusion during 11 years of observation, induced by a brief but intense period of apparent leopard predation. Before fusion, both groups made few incursions into the other groups territory and spent most of the time in their own territories. After the fusion, the amalgamated group shifted its activities and used both territories in similar proportion. Rates of female agonism increased after fusion, particularly in the 2 weeks following fusion, and the small group females assumed the lowest ranks in the female dominance hierarchy. Rates of agonism returned to prefusion rates a month later. Although rates of high‐intensity interactions (i.e., chases) did not increase after fusion, small group females were more likely to be the recipients of, and lose, agonistic interactions than large group females; a small group female and her infant were attacked and wounded by a coalition of large group females shortly after the fusion. The observations presented here reveal that the circumstances surrounding group fusions are more variable than previously realized, but are still in accordance with expectations from socio‐ecological theory that predation can favor the formation of larger groups. In this case, under threat of severe predation, individuals may have surrendered group autonomy for the greater security of larger numbers. Am. J. Primatol. 72:634–644, 2010.

Erratum to: Demography and Life Histories of Sympatric Patas Monkeys, Erythrocebus patas

In the original Fig. 1, the callitrichids were inadvertently omitted, not just the strepsirrhines as stated in the text. We correct this with a revised figure that includes all primates for which we have data. Because the residuals are calculated from a new regression (additional data points), their absolute values shift slightly; nonetheless, the pattern remains the same: vervets lie very near the regression line of rm versus ln body size (residuals near zero), whereas patas monkeys have a very high rm for their body size. The point to the right of the patas monkeys represents ruffed lemurs, Varecia variegata. Int J Primatol (2011) 32:268–269 DOI 10.1007/s10764-010-9444-0