Effect of Group Size on Time Budgets of Sichuan Snub-Nosed Monkeys (Rhinopithecus roxellana) in Shennongjia National Nature Reserve, China

Group size influences intragroup scramble competition, which in turn influences time budgets in some primates, and may impact age–sex classes differently. There is a great deal of debate about whether folivorous primates, e.g., colobines, experience significant feeding competition. Unlike most colobines, Sichuan snub-nosed monkeys (Rhinopithecus roxellana) live in extraordinarily large groups and eat mainly lichens supplemented by seasonal plant food. We examined the effect of group size on time budgets in this species by studying two groups of different sizes in the same habitat in Shennongjia National Nature Reserve, China (study periods: August 2006–July 2008 for the larger group, November 2008–July 2009 for the smaller group). Results showed that the distribution of activities throughout the day did not differ between groups, but that time budgets did differ. Specifically, the monkeys spent more time moving and less time resting in the larger group than in the smaller group. Intergroup comparisons for each age–sex class indicated that adult females (but not adult males or juveniles) in the larger group spent more time moving and less time resting, and tended to spend more time feeding compared to those in the smaller group. The results suggested that increased scramble competition was occurring for adult females in the larger group. We provided preliminary evidence for the existence of intragroup scramble competition in Rhinopithecus roxellana.     

Patch depletion behavior differs between sympatric folivorous primates

Food competition in group-living animals is commonly accepted as a critical determinant of foraging strategies and social organization. Here we examine food patch depletion behavior in a leaf-eating (folivorous) primate, the guereza (Colobus guereza). Snaith and Chapman (2005) studied the sympatric folivorous red colobus (Procolobus rufomitratus), which shares many food resources with the guereza. They determined that red colobus deplete the patches (feeding trees) they use, while we found contrary evidence for guerezas using the same methods. We found that the time guerezas spent feeding in a patch was affected by neither tree size, an indicator of food abundance, nor the size of the feeding group, an indicator of feeding competition. For their principal food item (young leaves), intake rate remained constant and coincided with a decrease in the distance moved to find food within a patch, implying that guerezas do not deplete patches. This points to a fundamental difference in the use of food by guerezas and red colobus, which may be linked to the large difference in their group sizes and/or to a disparity in their digestive physiologies. However, further analyses revealed that the number of feeders within a patch did not affect patch depletion patterns in either species, leaving the potential for a physiological basis as the most plausible explanation. Our research highlights the need for a more critical examination of folivorous primate feeding ecology and social behavior, as all folivorous primates are typically lumped into a single category in socioecological models, which may account for conflicting evidence in the literature.     

Predicting group size in primates: foraging costs and predation risks

We present a direct test of the long-standing hypothesis thatfood competition limits primate group size. Group size is acritical social variable because it constrains most other aspectsof social organization. We develop a simple population-specificindex of indirect feeding competition based on daily foragingcosts. This index explains nearly two-thirds of between-populationvariation in mean group sizes of mostly fruit-eating (but notof mostly leaf-eating) primates. Group size is also significantlyrelated to body size and terrestriality (or use of open country),which are suspected correlates of predation risk, although feedingcompetition remains an important predictor of group size evenwhen these correlates are controlled. Phylogeny also appearsto be important: the differences between observed mean populationgroup sizes and those predicted using ecological factors aremost positive for the Old World monkeys and most negative forthe lemuroids in our sample. The weak relationship between groupsize and feeding competition found for folivorous species maybe explained either by the energetic constraints of a leafydiet or by limits to group size imposed by infanticide as ahabitual male reproductive strategy.     

Impact of group size on female reproductive success of free-ranging Rhinopithecus roxellana in the Qinling Mountains, China

Group size influences female reproductive success through scramble/contest feeding competition, predation pressures and infanticide risks in primates. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is an endangered folivorous colobine species living in a multilevel society. From 2002 to 2008, we studied a free-ranging band of R. roxellana in the Qinling Mountains of China to examine the effect of group size on female reproductive success. During our observation period, the number of monkeys in the study band fluctuated from 61 to 108, and the number of one-male/multi-female groups within it varied from 7 to 10. A significant negative linear relationship was found between group size and birth rate, but group size was not significantly correlated with infant survival rate or interbirth interval. These results suggest that group size influences female reproductive success via within-group scramble competition in this folivorous species.     

Home-Range Use and Activity Patterns of the Red Langur (Presbytis rubicunda) in Sabangau Tropical Peat-Swamp Forest, Central Kalimantan, Indonesian Borneo

Knowledge of a species’ ranging patterns is vital for understanding its behavioral ecology and vulnerability to extinction. Given the abundance and even distribution of leaves in forested habitats, folivorous primates generally spend less time feeding; more time resting; have shorter day ranges; and require smaller home ranges than frugivorous primates. To test the influence of frugivory on ranging behavior, we established the activity budget and home-range size and use in a highly frugivorous population of the Borneo-endemic colobine, Presbytis rubicunda, within Sabangau tropical peat-swamp forest, Central Kalimantan, and examined relationships between fruit availability and ranging patterns. We collected 6848 GPS locations and 10,702 instantaneous focal behavioral scans on a single group between January and December 2011. The group had the largest home-range size recorded in genus Presbytis (kernel density estimates: mean = 108.3 ± SD 3.8 ha, N = 4 bandwidths). The annual activity budget comprised 48 ± SD 4.0% resting; 29.3 ± SD 3.9% feeding, 14.2 ± SD 2.5% traveling, and 0.4 ± SD 0.4% social behaviors. Mean monthly day-range length was the highest recorded for any folivorous primate (1645 ± SD 220.5 m/d). No significant relationships existed between ranging variables and fruit availability, and ranging behaviors did not vary significantly across seasons, potentially owing to low fluctuations in fruit availability. Our results suggest that colobine monkeys maintain larger than average ranges when high-quality food resources are available. Their extensive range requirements imply that protecting large, contiguous tracts of habitat is crucial in future conservation planning for Presbytis rubicunda.     

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 Fisher's 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.     

Habitat,diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1806)

Results of a 10-month study of the ecology and behavior of free- ranging woolly spider monkeys (Brachyteles arachnoides)in Brazil show that these animals are strongly folivorous. Leaf-eating accounted for more than 50% of the total feeding time in all samples but one and accounted for more than 80% of the total feeding time in three samples. Mature foliage was routinely eaten. Woolly spider monkeys consistently spend more than 50% of each day quietly resting and sleeping. Animals travel little except when actively feeding and show low levels of social interaction. Such an activity profile suggests that woolly spider monkeys may often be living near the limits of their energetic resources. The social organization of the species is unusual for a folivorous primate in that small groups of females and associated immature animals confine their activities to discrete home-range areas, whereas males are itinerant, traveling over the home ranges of various female groups. Animals sharing a common home-range area show no permanent daily pattern of association other than that of mother-dependent offspring. Foraging alone or with few conspecifics should maximize each individual’s returns from foraging by minimizing the day range that must be traveled each day to locate foods while simultaneously lowering interference competition for higher-quality dietary resources.     

Behavioral modifications in northern bearded saki monkeys (<Emphasis Type="Italic">Chiropotes satanas chiropotes</Emphasis>) in forest fragments of central Amazonia

We investigated behavioral differences among seven groups of northern bearded saki monkeys (Chiropotes satanas chiropotes) living in five forest fragments and two areas of continuous forest at the Biological Dynamics of Forest Fragments Project study area, located approximately 80 km north of Manaus, Brazil. We collected data in six research cycles from July–August 2003 to January 2005–April 2006. When bearded saki monkeys were present in a study area, we followed the group from dawn until dusk for three consecutive days. Every 5 min, we conducted behavioral scans of all visible individuals. There was a positive relationship between forest size and group size, but animals in the small forest fragments lived at greater densities. Bearded saki monkeys in the smaller fragments spent more time resting, less time traveling, and less time vocalizing, but there was no relationship between forest size and the amount of time spent feeding. Our results indicate that the main behavioral differences among the groups are related to the amount of forest resources (e.g., fruit trees, space) available to the monkeys in the smaller fragments, as well as the resulting smaller group sizes. We stress the need to preserve large tracts of forest and provide connectivity between forest patches.     

Increasing browse and social complexity can improve zoo elephant welfare

While recent work has assessed how environmental and managerial changes influence elephant welfare across multiple zoos, few studies have addressed the effects of management changes within a single institution. In this paper, we examine how management changes related to social structure and diet affect the behavior of a group of zoo elephants over a 23‐month period while also considering underlying factors, such as time of day, hormonal cycle, and individual differences. We recorded individual behaviors using 2‐min scan samples during 60‐min sessions. We analyzed behavioral changes across several study variables using generalized linear mixed models. We found that increasing browse can improve opportunities for foraging throughout the day but may not be sufficient to reduce repetitive behaviors. We observed that increasing group size and integration of bulls with cows can lead to increased social interaction in African elephants. Our results highlight the importance of using multiple management alterations to address elephant welfare, and considering environmental factors, when making management decisions.     

How group size affects vigilance dynamics and time allocation patterns: the key role of imitation and tempo

In the context of social foraging, predator detection has been the subject of numerous studies, which acknowledge the adaptive response of the individual to the trade-off between feeding and vigilance. Typically, animals gain energy by increasing their feeding time and decreasing their vigilance effort with increasing group size, without increasing their risk of predation ('group size effect'). Research on the biological utility of vigilance has prevailed over considerations of the mechanistic rules that link individual decisions to group behavior. With sheep as a model species, we identified how the behaviors of conspecifics affect the individual decisions to switch activity. We highlight a simple mechanism whereby the group size effect on collective vigilance dynamics is shaped by two key features: the magnitude of social amplification and intrinsic differences between foraging and scanning bout durations. Our results highlight a positive correlation between the duration of scanning and foraging bouts at the level of the group. This finding reveals the existence of groups with high and low rates of transition between activities, suggesting individual variations in the transition rate, or 'tempo'. We present a mathematical model based on behavioral rules derived from experiments. Our theoretical predictions show that the system is robust in respect to variations in the propensity to imitate scanning and foraging, yet flexible in respect to differences in the duration of activity bouts. The model shows how individual decisions contribute to collective behavior patterns and how the group, in turn, facilitates individual-level adaptive responses.     

The Effect of Climatic Factors on the Activity Budgets of Barbary Macaques (Macaca sylvanus)

Climatic conditions can significantly affect the behavior of animals and constrain their activity or geographic distribution. Barbary macaques (Macaca sylvanus) are one of the few primates that live outside the tropics. Here we analyze if and how the activity budgets of Barbary macaques are affected by climatic variables, i.e., air temperature, relative humidity, rainfall, and snow coverage. We collected scan sampling data on the activity budgets of four groups of macaques living in the Middle Atlas Mountains of Morocco from June 2008 to January 2011. This habitat is characterized by extreme seasonal changes, from cold and snowy winters to hot and dry summers. The activity budgets of the macaques differed across months but not across the time of day (with the exception of time spent feeding). The monkeys spent significantly more time feeding or foraging when there was no snow than when snow coverage was moderate or major. Daily rainfall was positively related to resting time and negatively to time spent moving or in social behavior. Air temperature was negatively related to time spent feeding or foraging. Finally, time spent on social behavior was significantly lower when relative humidity was high. These data indicate that environmental factors significantly affect the time budgets of endangered Barbary macaques, a species that has been little studied in the wild. Our findings support previous studies on temperate primates in showing that snow coverage can have negative consequences on the feeding ecology and survival of these species.     

Bigger groups have fewer parasites and similar cortisol levels: a multi-group analysis in red colobus monkeys

If stress and disease impose fitness costs, and if those costs vary as a function of group size, then stress and disease should exert selection pressures on group size. We assessed the relationships between group size, stress, and parasite infections across nine groups of red colobus monkeys (Procolobus rufomitratus) in Kibale National Park, Uganda. We used fecal cortisol as a measure of physiological stress and examined fecal samples to assess the prevalence and intensity of gastrointestinal helminth infections. We also examined the effect of behaviors that could potentially reduce parasite transmission (e.g., increasing group spread and reducing social interactions). We found that cortisol was not significantly related to group size, but parasite prevalence was negatively related to group size and group spread. The observed increase in group spread could have reduced the rate of parasite transmission in larger groups; however, it is not clear whether this was a density-dependent behavioral counter-strategy to infection or a response to food competition that also reduced parasite transmission. The results do not support the suggestion that gastrointestinal parasitism or stress directly imposed group-size-related fitness costs, and we cannot conclude that they are among the mechanisms limiting group size in red colobus monkeys.     

The effect of social and ecological factors on the time budget of wild vervet monkeys

Animals often have a limited time to perform different fitness‐enhancing activities, such as the trade‐off between socializing versus foraging in group‐living species. Many previous studies have focused on how ecological and social factors influence activity budget at the individual or group level in various species. However, few primate studies have focused on multiple study groups living within a similar habitat. Here, we analyse group, season and sex effects on the individual activity budget of wild vervet monkeys (Chlorocebus pygerythrus) living in four groups with overlapping home ranges. Generally, our findings support previous studies on primates. Our results indicate that intragroup competition may force larger groups to spend more time feeding and less time resting. We also found that seasonal variation, and therefore food availability, has a strong influence on the monkeys’ activity budget. Females, which are the philopatric sex in vervet monkeys, spent more time socializing while, in general, males spent more time resting. However, we did not find any difference on the time spent socializing between groups. Since there is evidence that not only time constraints and habitat quality but also group size influence individual behaviours and ultimately group living, we advise that future studies should focus on multiple groups of the same species living in the same habitat in order to better understand how all these variables are interlinked.     

Feeding rates and daily path range of the Colombian woolly monkeys as evidence for between- and within-group competition

Data on fruit feeding rates and daily path length were compared for four groups of woolly monkeys in Tinigua National Park, Colombia. Indirect evidence was found for feeding competition both within and between groups. Feeding rates were similar across groups of different sizes, but daily path lengths were longer in small and large groups when compared to medium-sized groups. The results suggest that the optimal group size in this study site is close to 20 individuals. Although the sample size was small and it was difficult to assess the influence of home range quality in some of the comparisons, this is one of the few studies providing empirical evidence supporting the importance of intergroup competition affecting group size in primates.     

Time Constraints Limit Group Sizes and Distribution in Red and Black-and-White Colobus

Researchers have shown that, in frugivorous primates, a major constraint on group size is intra group feeding competition. The relationship is less obvious in folivorous primates. We investigated whether colobine group sizes are constrained by time limitations as a result of their low energy diet and ruminant-like digestive system. We used climate as an easy to obtain proxy for the productivity of a habitat. Using the relationships between climate, group size, and time budget components for populations of Colobus and Piliocolobus at different research sites, we created 2 taxon-specific models. In both genera, feeding time increased with group size or biomass. The models for Colobus and Piliocolobus correctly predicted the presence or absence of the genera at, respectively, 86% of 148 and 84% of 156 African primate sites. Median predicted group sizes where the respective genera were present are 19 for Colobus and 53 for Piliocolobus. We show that the differences between the 2 genera are due mainly to intrinsic differences in the way each taxon’s digestive physiology interacts with climatic variables to influence resting time requirements. The models may help us explore their responses to climatic change in both the past and the future.     

Feeding Competition and Group Size in Alouatta pigra

Researchers consider group size in primates to be determined by complex relationships among numerous ecological forces. Antipredator benefits and better resource defense are the primary pressures for large groups. Conversely, intragroup limited food availability, can result in greater intragroup feeding competition and individual energy expenditure in larger groups, creating energetic advantages for individuals in small groups and placing an upper limit group size. However, the extent to which food availability constrains group size remains unclear for many species, including black howlers (Alouatta pigra), which ubiquitously live in small social groups (≤10 individuals). We studied the relationship between group size and 2 key indices of feeding competition—day journey length and activity budgets—in 3 groups of wild Alouatta pigra at a hurricane-damaged site in Belize, Central America. We controlled for differences in food availability between home ranges (food tree density) and compared both indicators of feeding competition directly with temporal variation in food availability for each group. Our results show no consistent association between resource availability, group size, and either index of competition, indicating that feeding competition does not limit group size at the site—i.e., that larger groups can form without increased costs of feeding competition. The results support the search for other explanations, possibly social ones, for small group size in the primates, and we conclude with suggestions and evidence for such alternative explanations.     

Universal behaviors as candidate traditions in wild spider monkeys

Candidate traditions were documented across three communities of wild spider monkeys (Ateles geoffroyi) using an a priori approach to identify behavioral variants and a statistical approach to examine differences in their proportional use. This methodology differs from previous studies of animal traditions, which used retrospective data and relied on the 'exclusion method' to identify candidate traditions. Our a priori approach increased the likelihood that behavior variants with equivalent functions were considered and our statistical approach enabled the proportional use of 'universal' behaviors, i.e., used across all communities, to be examined for the first time in any animal species as candidate traditions. Among universal behaviors we found 14 'community preferred' variants. After considering the extent to which community preferred variants were due to ecological and, to a lesser degree, genetic differences, we concluded that at least six were likely maintained through social learning. Our findings have two main implications: (i) tradition repertoires could be larger than assumed from previous studies using the exclusion method; (ii) the relative use of universal behavior variants can reinforce community membership.     

The Ranging Costs of a Fallback Food: Liana Consumption Supplements Diet but Increases Foraging Effort in Howler Monkeys

Lianas are important components in the dynamics of tropical forests and represent fallback foods for some primates, yet little is known about their impact on primate ecology, behavior or fitness. Using 2 yr of field data, we investigated liana consumption and foraging effort in four groups of howler monkeys (two in bigger, more conserved forest fragments and two in smaller, less conserved fragments) to assess whether howler monkeys use lianas when and where food availability is scarce, and how liana consumption is related to foraging effort. Howler monkeys in smaller fragments spent more time consuming lianas and liana consumption was negatively related to the consumption of preferred food resources (fruit and Ficus spp.). Further, travel time was positively related to liana feeding time, but not to tree feeding time, and howler monkeys visited a greater number of food patches when feeding from liana leaves than when feeding from tree leaves. Our results suggest that these increases in foraging effort were related to the fact that lianas are mainly a source of leaves, and that liana patch size was probably smaller than tree patch size. While these results were clear when analyzing all four groups combined, however, they were not always significant in each of the groups individually. We suggest that this may be related to the differences in group size, patch size and the availability of resources among groups. Further studies are necessary to assess whether these dietary and behavioral adjustments negatively impact on the fitness and conservation of primates in fragments.     

Balancing contest competition,scramble competition,and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus)

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within‐group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as “single female dominance,” with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.