Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal ...effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.
Mothers time spent grooming with subjects during infancy predicted subjects’ time grooming with any partner and with peers as juveniles. Further, mothers time spent grooming with peers during subjects’ infancy predicted subjects’ time playing with peers as juveniles. In both instances, males increased affiliative behavior with increased maternal affiliation, and females decreased.
HIGHLIGHTS
Mothers time spent grooming with subjects during infancy predicted subjects’ time grooming with any partner and with peers as juveniles.
Mothers time spent grooming with peers during subjects’ infancy predicted subjects’ time playing with peers as juveniles.
For both maternal effects, male and female juvenile behavior showed opposite responses.
Juvenile behavior predicted by early life mother sociality was not predicted by mothers sociality averaged over subjects’ lifetime.
Many tropical animals inhabit mosaic landscapes including human‐modified habitat. In such landscapes, animals commonly adjust feeding behavior, and may incorporate non‐natural foods. These behavioral ...shifts can influence consumers' nutritional states, with implications for population persistence. However, few studies have addressed the nutritional role of non‐natural food. We examined nutritional ecology of wild blue monkeys to understand how dietary habits related to non‐natural foods might support population persistence in a mosaic landscape. We documented prevalence and nutritional composition of non‐natural foods in monkey diets to assess how habitat use influenced their consumption, and their contribution to nutritional strategies. While most energy and macronutrients came from natural foods, subjects focused non‐natural feeding activity on five exotic plants, and averaged about a third of daily calories from non‐natural foods. Most non‐natural food calories came from non‐structural carbohydrates and least from protein. Consumption of non‐natural foods related to time in human‐modified habitats, which two groups used non‐randomly. Non‐natural and natural foods were similar in nutrients, and the amount of non‐natural food consumed drove variation in nutritional strategy. When more daily calories came from non‐natural foods, females consumed a higher ratio of non‐protein energy to protein (NPE:P). Females also prioritized protein while allowing NPE:P to vary, increasing NPE while capitalizing on non‐natural foods. Overall, these tropical mammals achieved a similar nutrient balance regardless of their intake of non‐natural foods. Forest and forest‐adjacent areas with non‐natural vegetation may provide adequate nutrient access for consumers, and thus contribute to wildlife conservation in mosaic tropical landscapes.
Wildlife in human‐altered mosaic habitats may eat non‐natural foods, but little is known about the nutritional implications of such behavior. This study documents how forest‐dwelling monkeys consume a third of their calories from non‐natural foods (mainly exotic plants), yet are able to achieve a similar nutrient balance regardless of exposure to and intake of these foods. Forest and forest‐adjacent areas with non‐natural vegetation may extend or enrich suitable habitat in terms of nutrient access for consumers, and thus contribute to wildlife conservation.
Generalist primates eat many food types and shift their diet with changes in food availability. Variation in foods eaten may not, however, match variation in nutrient intake. We examined dietary ...variation in a generalist‐feeder, the blue monkey (Cercopithecus mitis), to see how dietary food intake related to variation in available food and nutrient intake. We used 371 all‐day focal follows from 24 adult females (three groups) in a wild rainforest population to quantify daily diet over 9 months. We measured food availability using vegetation surveys and phenology monitoring. We analyzed >700 food and fecal samples for macronutrient content. Subjects included 445 food items (species‐specific plant parts and insect morphotypes) in their diet. Variation in fruit consumption (percentage of diet and total kcal) tracked variation in availability, suggesting fruit was a preferred food type. Fruits also constituted the majority of the diet (by calories) and some fruit species were eaten more than expected based on relative availability. In contrast, few species of young leaves were eaten more than expected. Also, subjects ate fewer young leaves (based on calories consumed) when fruit or young leaves were more available, suggesting that young leaves served as fallback foods. Despite the broad range of foods in the diet, group differences in fiber digestibility, and variation that reflected food availability, subjects and groups converged on similar nutrient intakes (grand mean ± SD: 637.1 ± 104.7 kcal overall energy intake, 293.3 ± 46.9 kcal nonstructural carbohydrate, 147.8 ± 72.4 kcal lipid, 107.8 ± 12.9 kcal available protein, and 88.1 ± 17.5 kcal structural carbohydrate; N = 24 subjects). Thus, blue monkeys appear to be food composition generalists and nutrient intake specialists, using flexible feeding strategies to regulate nutrient intake. Findings highlight the importance of simultaneously examining dietary composition at both levels of foods and nutrients to understand primate feeding ecology.
HIGHLIGHTS
Adult female blue monkeys in western Kenya preferred fruit and ate young leaves as fallback food.
Subjects in three groups consumed 445 categories of food items over 9 months.
The monkeys’ diverse, flexible diets converged on similar nutrient intakes across individuals, groups and seasons.
Abstract
Animals make dietary choices to achieve adequate nutrient intake; however, it is challenging to study such nutritional strategies in wild populations. We explored the nutritional strategy of ...a generalist social primate, the blue monkey (Cercopithecus mitis). We hypothesized that females balance intake of nutrients, specifically non-protein energy and protein, both on a daily and long-term basis. When balancing was not possible, we expected subjects to prioritize constant protein intake, allowing non-protein energy to vary more. To understand the ecology of nutrient balancing, we examined how habitat use, food availability, diet composition, social dominance rank, and reproductive demand influenced nutrient intake. Over 9 months, we conducted 371 all-day focal follows on 24 subjects in Kakamega Forest, Kenya. Females exhibited short- and long-term nutritional strategies. Daily, they balanced non-protein energy to protein intake but when balancing was impossible, monkeys prioritized protein intake. Longer term, they balanced non-protein energy:protein intake in a 3.8:1 ratio. The ratio related positively to fruit in the diet and negatively to time in near-natural forest, but we found no evidence that it related to food availability, reproductive demand, or dominance rank. Lower-ranked females had broader daily diets, however, which may reflect behavioral feeding strategies to cope with social constraints. Overall, females prioritized daily protein, allowing less variation in protein intake than other aspects such as non-protein energy:protein ratio and non-protein energy intake. The emerging pattern in primates suggests that diverse dietary strategies evolved to allow adherence to a nutrient balance of non-protein energy:protein despite various social and environmental constraints.
Animals must make dietary choices to achieve adequate nutrient intake, but studying nutrient strategies is challenging in the field. Using behavioral and laboratory data, we show that a generalist primate, the blue monkey, used distinct daily and long-term strategies to achieve such intake. Daily, female subjects prioritized consuming protein (i.e., maintained relatively constant intake). Over multiple months, however, subjects balanced intake of non-protein energy (carbohydrates and fat) and protein, despite potential environmental and social constraints.
AbstractWhile blue monkey groups often defend feeding territories against their neighbours, group members do not participate equally. Data spanning 5 years and 5 wild groups were used to address ...factors that might explain variable participation, both across age-sex classes and among individual adult females. Adult females participated most, although there was a 9-fold difference between those individuals who participated most and least. Juvenile participation increased with age, but female juveniles participated more than males in each cohort. Male juveniles reduced participation as they approached the age of natal emigration. In general, it seems that adult participation patterns are acquired gradually during ontogeny. Among adult females, those with infants participated less than those without infants, and higher-ranking females participated more than lower-rankers. The presence of matrilineal kin in the group did not generally affect participation by adult females. Age-sex class differences and the effect of infant presence can be explained in terms of relative costs and benefits to participation. The lack of a kinship effect was unexpected. The rank effect was also unanticipated, given that rank does not predict reproductive success in this species. High-ranking females may face lower costs, offer staying incentives to lower-ranked females, or trade services with them.
Comparative data from wild populations are necessary to understand the evolution of primate life history strategies. We present demographic data from a 29-yr longitudinal study of 8 groups of ...individually recognized wild blue monkeys (Cercopithecus mitis stuhlmanni). We provide estimates of life history variables and a life table for females. Most females had their first infant at 7 yr. The mean interbirth interval was 28 mo, and decreased from 31 to 18 mo if the first infant died within a year. Interbirth intervals did not differ according to infant sex, but females had longer intervals after their first vs. subsequent births. Infant mortality was 23% and did not differ strongly by sex or mother's parity. Maximal female lifespan was 32.5-34.5 yr. Across the lifespan, both survivorship and fecundity showed typical primate patterns. Survivorship was lowest in infants, leveled off among juveniles, and then decreased gradually with increasing age in later life. Fecundity was highest among young females and decreased among older females. Births were seasonal, with 64% occurring within 3 mo at the end of the dry season and beginning of the wet season. Survival to 12 mo was higher for infants born during drier months. Birth season timing is plausibly related to thermoregulation of infants, weanling foods, or maternal energy demand. Blue monkeys are a forest-dependent species with a very slow life history and relatively low immature and adult mortality rates compared to closely related guenons living in open habitats. Even among cercopithecines as a whole, they appear to have an exceptionally slow life history relative to body size. Differences in life history “speed” between blue monkeys and their close relatives seem to be related to lower juvenile and adult mortality in forests relative to more open habitats.
To investigate the selective agents that shape signals, we examined function (adaptive benefit to signaler) in the boom loud call by male blue monkeys. Using natural observation and playbacks in a ...wild population in Kenya, we characterized boom function from conspecifics' behavioral responses and also variation in call usage relating to context and reproductive season. Booms occurred in several contexts and after varied stimuli, including falling branches, yet were strongly associated with intragroup activity and, in particular, affiliative interactions between callers and females. Males produced more booms during the mating season and, congruently, when more females in their groups were sexually active. After hearing booms, compared to no call, females spent more time near groupmates and the caller and were more likely to approach and have mating interactions with him. Males tended to move away after hearing a boom. In the aggregate, results indicate that booms achieve multiple functions relating to facilitating group cohesion, affiliative interactions, and mating opportunities, while also repelling rival males. An observed association with falling branches is puzzlingly distinct from these social functions. We explore the hypothesis that booms enable affiliative encounters by acting as signals of benign intent, and discuss the functional versatility of signals perceived by multiple receivers that vary in age, sex, and relationship to signalers.
Previous studies have shown that the number, noise level, and activity level of zoo visitors can negatively influence the behavior of captive animals. This study combined these three factors into a ...single visitor impact score and assessed whether visitor impact predicted the frequency or occurrence of displacement activities, affiliative behaviors, and aggression in a group of six captive ebony langurs (
Trachypithecus auratus
). This study also examined whether the amount of time the ebony langurs spent sleeping each day was correlated to the mean visitor impact score for that day. We used negative binomial and binomial models to analyze data collected during 5-min focal follows. Higher visitor impact scores predicted greater expression of displacement activities, affiliative behaviors, and aggression, suggesting that zoo visitors were a source autonomic arousal for the langurs. Similarly, the langurs spent more time sleeping on days with higher mean visitor impact scores, which may indicate learned helplessness. This study suggests that zoo visitors may be a source of environmental stress for captive ebony langurs. Nevertheless, the positive relationship between high visitor impact score and the occurrence of affiliative behavior types may indicate that the langurs use certain activities to decrease visitor-induced stress.
Vigilance behaviour is often viewed as a predation avoidance strategy, but animals also use visual monitoring to detect conspecific threats. Studies of social vigilance often consider how group size ...or nearby conspecifics influence vigilance levels. Less is known about how more specific social variables, such as relative rank and kinship of a subject’s neighbours, affect vigilance of wild animals along with predation risk. To evaluate alternative functional hypotheses for vigilance behaviour, including predator detection and both extra- and within-group conspecific monitoring, we investigated how predation risk and social factors account for variation in vigilance in wild blue monkeys, Cercopithecus mitis, which show strong aggressive competition between groups and mild aggression within them. Studying 18 adult females in two groups, we measured time spent vigilant in 90s focal samples, recording the subject's activity, microhabitat conditions and identity of neighbours. We used data on dominance ranks and kinship to assess subject-specific social context for each sample. We compared generalized linear mixed models corresponding to each hypothesized function of vigilance, relating variation in vigilance to factors associated with a particular function. The best model related vigilance to predictor variables of all three functions, including recency of an antipredator event, height in canopy, position in forest (edge/interior), recency of an intergroup encounter, number of nearby kin, subject rank and presence of high-ranking neighbours. Overall, most variation in vigilance related to predation risk and between-group competition, while within-group social factors had smaller effects. The range of predictors suggests that vigilance behaviour serves multiple functions, including predator detection and both extragroup and intragroup conspecific monitoring. Species with different social systems might be expected to show different balances of factors that influence vigilance behaviour.
► Predation risk and social factors influence vigilance in wild blue monkeys. ► The primary function of vigilance in blue monkeys is most likely predator detection. ► The identities, but not number, of neighbours influenced vigilance duration. ► In a mildly aggressive species, social monitoring is a minor component of vigilance. ► Social systems may explain interspecific variation in functions of vigilance.
Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life ...span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.
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