Gastrointestinal parasites of critically endangered primates endemic to Tana River, Kenya: Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus)

We conducted fecal egg counts of gastrointestinal parasites of 2 critically endangered primates endemic to the forest of Tana River, Kenya. We aimed to use the fecal egg counts as proxies to quantify the prevalence of gastrointestinal parasites between the 2 primates. The Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus) are of similar body size, but their behavioral ecology is very different. We predicted that mangabeys would have a higher prevalence of parasites because they are mostly terrestrial omnivores, live in larger social groups, and therefore range widely. We detected 10 nematodes and 3 protozoans in mangabeys and 7 nematodes and 2 protozoans in colobus. We detected a higher number of different parasite species in individual mangabeys, and 4 of the 5 nematodes requiring intermediate hosts were found in mangabeys. The overall prevalence of parasites was higher for mangabeys, but this difference was not statistically significant. For colobus, we found a trend whereby the number of different parasite species in individual monkeys was higher in males and in lactating females. However, there was no difference in the prevalence of parasites between the sexes or between lactating and nonlactating females.     

Gastrointestinal parasites of the colobus monkeys of Uganda

From August 1997 to July 2003, we collected 2,103 fecal samples from free-ranging individuals of the 3 colobus monkey species of Uganda-the endangered red colobus (Piliocolobus tephrosceles), the eastern black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus (C. angolensis)--to identify and determine the prevalence of gastrointestinal parasites. Helminth eggs, larvae, and protozoan cysts were isolated by sodium nitrate flotation and fecal sedimentation. Coprocultures facilitated identification of helminths. Seven nematodes (Strongyloides fulleborni, S. stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 3 protozoans (Entamoeba coli, E. histolytica, and Giardia lamblia) were detected. Seasonal patterns of infection were not apparent for any parasite species infecting colobus monkeys. Prevalence of S. fulleborni was higher in adult male compared to adult female red colobus, but prevalence did not differ for any other shared parasite species between age and sex classes.     

Do food availability,parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?

Identifying factors that influence animal density is a fundamental goal in ecology that has taken on new importance with the need to develop informed management plans. This is particularly the case for primates as the tropical forest that supports many species is being rapidly converted. We use a system of forest fragments adjacent to Kibale National Park, Uganda, to examine if food availability and parasite infections have synergistic affects on red colobus (Piliocolobus tephrosceles) abundance. Given that the size of primate populations can often respond slowly to environmental changes, we also examined how these factors influenced cortisol levels. To meet these objectives, we monitored gastrointestinal parasites, evaluated fecal cortisol levels, and determined changes in food availability by conducting complete tree inventories in eight fragments in 2000 and 2003. Red colobus populations declined by an average of 21% among the fragments; however, population change ranged from a 25% increase to a 57% decline. The cumulative basal area of food trees declined by an average of 29.5%; however, forest change was highly variable (a 2% gain to a 71% decline). We found that nematode prevalence averaged 58% among fragments (range 29-83%). The change in colobus population size was correlated both with food availability and a number of indices of parasite infections. A path analysis suggests that change in food availability has a strong direct effect on population size, but it also has an indirect effect via parasite infections.     

Do Nematode Infections of Red Colobus (Procolobus rufomitratus) and Black-and-White Colobus (Colobus guereza) on Humanized Forest Edges Differ from Those on Nonhumanized Forest Edges?

Forested edges, especially those that border humanized landscapes, provide opportunities for nonhuman primates and people to interact, and such interactions are predicted to alter disease dynamics. Given the rapid expansion of edge habitats globally, understanding changes occurring on edges is important in evaluating primate behavioral ecology and developing conservation plans. Our research investigates predictions concerning how gastrointestinal parasite and stress levels (cortisol) in red colobus and black-and-white colobus (Procolobus rufomitratus; Colobus guereza) in Kibale National Park, Uganda, differ between humanized and nonhumanized forest edges. We found Trichuris sp., an unidentified strongyle, and Strongyloides sp. in the fecal samples. Results did not generally support our expectation that humanized forest edges increase parasite infection and, counter to what we predicted, fecal cortisol did not differ between habitats, suggesting that proximity to edges and/or to humans did not result in increased stress. We conclude that broad habitat classifications, e.g., “humanized,” may be too general to identify consistent differences in parasite infection, as other factors, specific to the parasite (e.g., life cycled), host (e.g., immune systems strength), or environment (e.g., moisture level), likely also play important roles.     

Parasite prevalence and richness in sympatric colobines: effects of host density

Factors that influence proximity and the number and duration of contacts among individuals can influence parasite transmission among hosts, and thus parasite prevalence and species richness are expected to increase with increasing host density. To examine this prediction we took advantage of a unique situation. Following the clearing of a forest fragment that supported red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza), the animals moved into a neighboring fragment that we had been monitoring for a number of years and for which we had described the primate parasite community. After the animals immigrated into the fragment, the colobus populations more than doubled and colobus density became almost twice that found in Kibale National Park, Uganda. Despite this increase in host density, the richness of the parasite community did not increase. However, in both colobus species the prevalence of Trichuris sp., the only commonly occurring gastrointestinal parasite, increased. Over the next 5 years the prevalence and intensity of infection of Trichuris sp. in red colobus declined and their population numbers slowly increased. In contrast, the prevalence and intensity of infection of Trichuris sp. increased in black-and-white colobus and remained high following the immigration, and their population size declined. While Trichuris sp. infections are typically asymptomatic, we consider it a possibility that they contributed to the decline of the black-and-white colobus, and that the red colobus may be serving as a reservoir for Trichuris, thereby increasing the infection risk for black-and-white colobus.     

Temporal dynamics of nutrition, parasitism, and stress in colobus monkeys: implications for population regulation and conservation

The need to develop conservation plans calls for the ability to identify ecological factors that influence population density. Because stress is known to affect fecundity and mortality, increasing stress may provide a warning of potential population declines. We examined the effects of temporal variation in nutrition and parasitism on stress in endangered red colobus monkeys in Kibale National Park, Uganda. First, we tested the hypothesis that parasitism and nutrition would individually affect stress levels. We found that periods of poor-quality diet corresponded with an increase in cortisol. Similarly, increases in parasite infections were associated with increased cortisol. Next, we predicted that a poor-quality diet would facilitate increased parasite infections, and that together, they would lead to amplified stress. However, we found no support for such amplification, likely because the quality of the diet had little effect on parasite infections. Third, we tested whether individuals in a larger group were subject to food stress due to greater within-group competition, which would intensify nutritional stress and parasitism, and lead to reduced reproduction. Although we found no evidence to support a group size effect on parasites, cortisol levels in the large group tended to be higher than those in the small group, and the large group had fewer infants per female. The results suggest that parasitism and poor nutrition lead to increased stress which, because they are known to be associated with reduced fecundity and increased mortality, may lead to population declines.     

Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups

Humans are responsible for massive changes to primate habitats, and one unanticipated consequence of these alterations may be changes in host-parasite interactions. Edges are a ubiquitous aspect of human disturbance to forest landscapes. Here we examine how changes associated with the creation of edges in Kibale National Park, Uganda, alter the parasite community that is supported by two species of African colobines: the endangered red colobus (Piliocolobus tephrosceles) and the black-and-white colobus (Colobus guereza). An analysis of 822 fecal samples from edge and forest interior groups revealed no difference in the richness of parasite communities (i.e., the number of parasite species recovered from the host's fecal sample). However, for both species the proportion of individuals with multiple infections was greater in edge than forest interior groups. The prevalence of specific parasites also varied between edge and forest interior groups. Oesophagostomum sp., a potentially deleterious parasite, was 7.4 times more prevalent in red colobus on the edge than in those in the forest interior, and Entamoeba coli was four times more prevalent in red colobus on the edge than in animals from the forest interior. Environmental contamination with parasites (measured as parasite eggs/gm feces) by red colobus from the edge and forest interior differed in a similar fashion to prevalence for red colobus, but it did not differ for black-and-white colobus. For example, egg counts of Oesophagostomum sp. were 10 times higher in red colobus from the edge than in those from the interior. The less severe infections in the black-and-white colobus relative to the red colobus may reflect the fact that black-and-white colobus raid agricultural crops while red colobus do not. This nutritional gain may facilitate a more effective immune response to parasites by the black-and-white colobus. The fact that animals on the edge are likely not nutritionally stressed raises an intriguing question as to what facilitates the elevated infections in edge animals. We speculate that interactions with humans may be linked to the observed patterns of infections, and hence that understanding the ecology of infectious diseases in nonhuman primates is of paramount importance for conservation and potentially for human-health planning.     

Group size in folivorous primates: ecological constraints and the possible influence of social factors

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobuss home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobuss home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Competing pressures on populations: long-term dynamics of food availability,food quality,disease, stress and animal abundance

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.     

Group Size Dynamics over 15+ Years in an African Forest Primate Community

Group size affects many aspects of the ecology and social organization of animals. We investigated group size stability for five primate species in Kibale National Park, Uganda from 1996 to 2011 at three nested spatial scales. Survey data indicated that group sizes did not change for most species, with the exception of red colobus monkeys (Procolobus rufomitratus), in which group size increased at all spatial scales. Mangabey (Lophocebus albigena) group size increased in old‐growth forest, but the sample size and increase were small. To augment this survey data, we collected several years of demographic data on three habituated groups of redtail monkeys (Cercopithecus ascanius), eight groups of black‐and‐white colobus (Colobus guereza), and one red colobus group. The red colobus group increased from 59 to 104 individuals, while redtail monkey and black‐and‐white colobus group sizes were stable, mirroring our survey results. To understand mechanisms behind group size changes in red colobus versus stability in other primates, we monitored forest dynamics at two spatial scales between 1990 and 2013, considered changes in predator population, and explored evidence of disease dynamics. The cumulative size of all trees and red colobus food trees increased over 24 yr, suggesting that changing food availability was driving group size changes for red colobus, while predation and disease played lesser roles. Overall, our results and evidence of changing primate densities suggest that the Kibale primate community is in a non‐equilibrium state. We suggest future conservation and management efforts take this into consideration.     

Estrogenic plant consumption predicts red colobus monkey (Procolobus rufomitratus) hormonal state and behavior

Numerous studies have examined the effects of anthropogenic endocrine disrupting compounds; however, very little is known about the effects of naturally occurring plant-produced estrogenic compounds (i.e., phytoestrogens) on vertebrates. To examine the seasonal pattern of phytoestrogen consumption and its relationship to hormone levels (407 fecal samples analyzed for estradiol and cortisol) and social behavior (aggression, mating, and grooming) in a primate, we conducted an 11-month field study of red colobus (Procolobus rufomitratus) in Kibale National Park, Uganda. The percent of diet from estrogenic plants averaged 10.7% (n = 45 weeks; range: 0.7–32.4%). Red colobus fed more heavily on estrogenic Millettia dura young leaves during weeks of higher rainfall, and the consumption of this estrogenic item was positively correlated to both their fecal estradiol and cortisol levels. Social behaviors were related to estradiol and cortisol levels, as well as the consumption of estrogenic plants and rainfall. The more the red colobus consumed estrogenic plants the higher their rates of aggression and copulation and the lower their time spent grooming. Our results suggest that the consumption of estrogenic plants has important implications for primate health and fitness through interactions with the endocrine system and changes in hormone levels and social behaviors.     

Physiological and Behavioral Effects of Capture Darting on Red Colobus Monkeys (Procolobus rufomitratus) with a Comparison to Chimpanzee (Pan troglodytes) Predation

Understanding how human activities affect wild primates is critical to the design of effective conservation strategies. Despite this need, few studies have examined the physiological and behavioral effects of field research methods in the wild. Here, we examine how the stress response, i.e., fecal cortisol, and behavior of Ugandan red colobus monkeys (Procolobus rufomitratus) in Kibale National Park are affected by chemical immobilization and collaring, i.e., capture. We compare this anthropogenic stressor to a naturally occurring stressor: a chimpanzee (Pan troglodytes) predation attack. Two adult males had peak cortisol levels of 283 and 284 ng/g 2–3 d after capture, which were 190% and 182% above their baseline levels, i.e., the first sample taken immediately after capture, but these peak levels did not remain elevated. Using long-term data, i.e., 11 mo of data, we found no difference in fecal cortisol levels between 10 darted and collared individuals and 14 individuals living in the same social group that were not darted or collared. For the chimpanzee attack, peak fecal cortisol levels (147–211% above baseline) were recorded 1–4 d after the attack, but these levels also did not remain elevated for long. These data show that darting and collaring and a chimpanzee predation attempt caused an acute stress response, but neither leads to sustained elevated cortisol levels. Thus, in situations in which research contributes significantly to the conservation of primates and cannot be conducted noninvasively, capture darting appears to be a useful technique with minimal long-term effects as long as injury and mortality are avoided. However, we encourage researchers to make similar physiological and behavioral comparisons in other field studies using similar techniques to provide a better understanding of the effects of research practices on the stress physiology and social behavior of wild primates.     

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. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Estrogenic plant consumption predicts red colobus monkey (Procolobus rufomitratus) hormonal state and behavior

Numerous studies have examined the effects of anthropogenic endocrine disrupting compounds; however, very little is known about the effects of naturally occurring plant-produced estrogenic compounds (i.e., phytoestrogens) on vertebrates. To examine the seasonal pattern of phytoestrogen consumption and its relationship to hormone levels (407 fecal samples analyzed for estradiol and cortisol) and social behavior (aggression, mating, and grooming) in a primate, we conducted an 11-month field study of red colobus (Procolobus rufomitratus) in Kibale National Park, Uganda. The percent of diet from estrogenic plants averaged 10.7% (n = 45 weeks; range: 0.7–32.4%). Red colobus fed more heavily on estrogenic Millettia dura young leaves during weeks of higher rainfall, and the consumption of this estrogenic item was positively correlated to both their fecal estradiol and cortisol levels. Social behaviors were related to estradiol and cortisol levels, as well as the consumption of estrogenic plants and rainfall. The more the red colobus consumed estrogenic plants the higher their rates of aggression and copulation and the lower their time spent grooming. Our results suggest that the consumption of estrogenic plants has important implications for primate health and fitness through interactions with the endocrine system and changes in hormone levels and social behaviors.     

Sickness behaviour associated with non-lethal infections in wild primates

Non-lethal parasite infections are common in wildlife, but there is little information on their clinical consequences. Here, we pair infection data from a ubiquitous soil-transmitted helminth, the whipworm (genus Trichuris), with activity data from a habituated group of wild red colobus monkeys (Procolobus rufomitratus tephrosceles) in Kibale National Park, Uganda. We use mixed-effect models to examine the relationship between non-lethal parasitism and red colobus behaviour. Our results indicate that red colobus increased resting and decreased more energetically costly behaviours when shedding whipworm eggs in faeces. Temporal patterns of behaviour also changed, with individuals switching behaviour less frequently when whipworm-positive. Feeding frequency did not differ, but red colobus consumption of bark and two plant species from the genus Albizia, which are used locally in traditional medicines, significantly increased when animals were shedding whipworm eggs. These results suggest self-medicative plant use, although additional work is needed to verify this conclusion. Our results indicate sickness behaviours, which are considered an adaptive response by hosts during infection. Induction of sickness behaviour in turn suggests that these primates are clinically sensitive to non-lethal parasite infections.     

Sociality, glucocorticoids and direct fitness in the communally rearing rodent, Octodon degus

While ecological causes of sociality (or group living) have been identified, proximate mechanisms remain less clear. Recently, close connections between sociality, glucocorticoid hormones (cort) and fitness have been hypothesized. In particular, cort levels would reflect a balance between fitness benefits and costs of group living, and therefore baseline cort levels would vary with sociality in a way opposite to the covariation between sociality and fitness. However, since reproductive effort may become a major determinant of stress responses (i.e., the cort–adaptation hypothesis), cort levels might also be expected to vary with sociality in a way similar to the covariation between sociality and fitness. We tested these expectations during three years in a natural population of the communally rearing degu, Octodon degus. During each year we quantified group membership, measured fecal cortisol metabolites (a proxy of baseline cort levels under natural conditions), and estimated direct fitness. We recorded that direct fitness decreases with group size in these animals. Secondly, neither group size nor the number of females (two proxies of sociality) influenced mean (or coefficient of variation, CV) baseline cortisol levels of adult females. In contrast, cortisol increased with per capita number of offspring produced and offspring surviving to breeding age during two out of three years examined. Together, our results imply that variation in glucocorticoid hormones is more linked to reproductive challenge than to the costs of group living. Most generally, our study provided independent support to the cort–adaptation hypothesis, according to which reproductive effort is a major determinant, yet temporally variable, influence on cort–fitness covariation.     

Dyadic associations of red Colobus and diana monkey groups in the Taï National Park, Ivory Coast

Members of the genus Colobus have been observed to associate frequently with Cercopithecus monkeys in several African sites. In the Taï National Park, Ivory Coast, one group of western red colobus was found to be in association with one particular group of diana monkeys more than could be expected by chance (Holenweg et al., 1996). We show that dyadic association is not an idiosyncrasy of these two groups, but rather a pattern that is general for our study site. All five red colobus groups we studied were closely associated with diana monkeys during more than 60% of the time. Four groups had one particular diana partner group, the fifth two different partners. Apart from the red colobus, three more primate species, the olive colobus, Campbell's monkey, and the lesser spot-nosed monkey, were also strongly attracted to diana monkeys.     

Monkey Abundance and Social Structure in Two High-Elevation Forest Reserves in the Udzungwa Mountains of Tanzania

The effects of human activity on population and social structure are a pantropical concern for primate conservation. We compare census data and social group counts from two forests in the Udzungwa Mountains, Tanzania. The main aim is to relate differences within and between the forests to current theory on the effect of human disturbance on primate abundance and group size. The survey reveals the presence of the restricted-range red colobus, Procolobus gordonorum, in New Dabaga/Ulangambi Forest Reserve (NDUFR). The primate community of NDUFR is impoverished compared to that in Ndundulu forest. Red colobus and black-and-white colobus (Colobus angolensis palliatus) abundance and group size are lowest in NDUFR. Fission-fusion of red colobus social groups may be occurring in previously logged areas of both forests. Our observations are consistent with current theory on the effect of habitat degradation and hunting on primates, but the relative effects of the 2 factors could not be differentiated. We pooled the results with previous data to show that abundance of red colobus in the Udzungwa Mountains is lowest at high elevations. Low red colobus group sizes appear to be related to human activity rather than elevation. Black-and-white colobus and Sykes monkeys (Cercopithecus mitis) show no relationship with elevation. Future studies will require more detailed information on vegetation, diet and ranging patterns to interpret fully intraspecific variation in population demography and social structure in the Udzungwa Mountains.     

Increasing Group Size Alters Behavior of a Folivorous Primate

Group size influences many aspects of mammalian social life, including stress levels, disease transmission, reproductive rates, and behavior. However, much of what is known about the effects of group size on behavioral ecology has come from comparisons across multiple groups of different sizes. These findings may be biased because behavioral differences across groups may be more indicative of how environmental variation influences animal behavior, rather than group size itself. To partially circumvent this limitation, we used longitudinal data to examine how changes in group size across time affect the behavior of folivorous red colobus monkeys (Procolobus rufomitratus) of Kibale National Park, Uganda. Controlling for food availability, we demonstrated that increasing group size resulted in altered activity budgets, based on 6 yr of data on a group that increased from 57 to 98 members. Specifically, as group size increased, individuals spent less time feeding and socializing, more time traveling, and increased the diversity of their diet. These changes appear to allow the monkeys to compensate for greater scramble competition apparent at larger group sizes, as increasing group size did not show the predicted relationship with lower female fecundity. Our results support recent findings documenting feeding competition in folivorous primates. Our results also document behavioral flexibility, an important trait that allows many social mammals to maximize the benefits of sociality (e.g., increased vigilance), while minimizing the costs (e.g., increased feeding competition).     

Optimal group size and seasonal stress in ring-tailed lemurs (Lemur catta)

Adaptive explanations for social grouping assume that thereare fitness consequences associated with group size, and individualsmaintain membership in groups of favorable size to maximizefitness. Here I examine fecal cortisol concentrations as a hormonalmeasure of stress to assess the relative well-being of Lemurcatta in groups of different size and in seasons of normal andlow tamarind fruit availability. I test the hypotheses thatthere is an optimal group size at which cortisol is lowest andthat optimal group size changes in food-scarce conditions. Icollected 799 fecal samples from 87 individuals in seven free-rangingL. catta groups at Berenty Reserve, Madagascar, over a 1-yearperiod (August 1999–July 2000) and determined fecal cortisolconcentrations using a radioimmunoassay. Expressing these asresiduals from monthly population means to control for temporalfluctuations in cortisol concentration, I calculated mean fecalcortisol levels for each animal in seasons of normal and lowtamarind fruit abundance and over the entire year. Overall,females exhibited lowest mean cortisol levels in groups of intermediatesize, suggesting that there are benefits to maintaining membershipin these groups. Females in groups that were atypically largeor small for their habitat type had higher mean cortisol levelsthan typical groups. Cortisol levels increased in food-scarceconditions for larger groups, suggesting that intergroup competitiveadvantages do not outweigh intragroup feeding competition atthis time. Group size may be optimized for long-term averageconditions, and short-term stresses may intermittently alterthe costs associated with group size.