Primate socioecology at the crossroads: Past, present, and future

Attempts to explain differences in the size and structure of primate groups have argued that they are a consequence of variation in the intensity of feeding competition caused by contrasts in food distribution. However, although feeding competition can limit the size of female groups, many other factors affect the costs and the benefits of sociality to females and contribute to differences in group size. Moreover, interspecific differences in social relationships between females, in female philopatry, and in kinship between group members appear to be more closely associated with variation in life‐history parameters, reproductive strategies, and phylogeny than with contrasts in food distribution or feeding competition. The mismatch between predictions of socioecological theory and observed variation in primate social behavior has led to protracted arguments about the future of primate socioecology. We argue that future attempts to understand the diversity of primate societies need to be based on an approach that explores separate explanations for different components of social organization, combines ecological and phylogenetic information, and integrates research on primates with similar studies of other groups of mammals. © 2012 Wiley Periodicals, Inc.     

Activity Patterns, Intergroup Encounters, and Male Affiliation in Free-Ranging Bearded Sakis (Chiropotes sagulatus)

The assessment of how primates divide their daily activities is one of the foundations of primate behavioral ecology but the activity patterns and social behavior of the Pitheciines, including bearded sakis (genus Chiropotes), are poorly understood. During a 15-mo study, I collected 560 h of data on subgrouping, activity patterns, social behavior, and intergroup encounters of a group of free-ranging Guianan bearded sakis (Chiropotes sagulatus) in Guyana. The study group consisted of at least 65 individuals but showed a high degree of flexibility in grouping patterns (mean group size 39 ± 10). They were highly active, spending ca. 70% of their diurnal activity budget traveling and feeding. Activity patterns were relatively consistent throughout the year, although time spent feeding correlated significantly with fruit availability. The most common social behaviors were social resting and grooming. Agonism was rare (2.56% of social behavior) but did occur in the context of intergroup encounters, with males from the same group cooperating in intergroup agonism. Bearded sakis showed a high level of within group male affiliation, with male–male partners making up 65% of grooming dyads and males having another male as their nearest-neighbor 66% of the time. These results show that bearded sakis are characterized by egalitarian male–male and male–female relationships, highly fluid group sizes, and high levels of male affiliation. Similarities in the social behavior of bearded sakis and muriquis suggest several possible explanations for male–male bonding including cooperative defense of females from other groups, kinship, and maintenance of social cohesion after subgroup coalescence.     

Male-male Interactions in Heterosexual and All-male Wild Mountain Gorilla Groups

Variation in male dispersal and behavior patterns are components of intraspecific differences in social systems. A comparison of male behavior in different social settings can be useful for determining which behavioral mechanisms contribute to variability in social systems. Two heterosexual multimale groups and one all-male group of mountain gorillas (Gorilla gorilla beringei) were observed for over 1100 h at the Karisoke Research Centre, Rwanda. Data on proximity patterns, dominance relationships, aggression, agonistic interventions, affiliation, and homosexual behavior were compared among the males in these groups to examine the influence of female presence, sex ratio, group size, and kinship on male—male interactions. Males in the all-male group stayed closer together, affiliated more, exhibited more homosexual behavior, and were more aggressive toward each other than males in heterosexual groups. However, the males in heterosexual groups showed more wounding and more consistent dominance relationships. Kinship did not influence male-male relationships in the all-male group. The males in the heterosexual groups rarely interacted with one another; they may actively avoid close proximity to reduce aggression. Results suggest that the variable social system of mountain gorillas may be more strongly influenced by demographic factors, male-female social relationships, and male-male competition for mates than by any benefits of male-male relationships.     

The dining etiquette of desert baboons: the roles of social bonds, kinship, and dominance in co-feeding networks

To better understand how individual relationships influence patterns of social foraging in primate groups, we explored networks of co-feeding in wild desert baboons (Papio ursinus). To minimize the risk of aggression and injury associated with contest competition, we expected that individual group members would choose to co-feed with those group-mates that are most likely to show tolerance and a willingness to share food patches. We tested two alternative hypotheses about who those group-mates might be: the "social bonds hypothesis" predicts that preferred foraging partners will be those with whom individuals share strong social bonds, indexed by grooming, whereas the "kinship hypothesis" predicts that preferred foraging partners will be relatives. We also investigated and controlled for the effects of dominance rank, given that competitive ability is known to shape foraging patterns. Social network analyses of over 5,000 foraging events for 14 adults in a single troop revealed that baboon co-feeding was significantly correlated with grooming relationships but not genetic relatedness, and this finding was also true of the female-only co-feeding network. Dominant individuals were also found to be central to the co-feeding network, frequently sharing food patches with multiple group-mates. This polyadic analysis of foraging associations between individuals underlines the importance of dominance and affiliation to patterns of primate social foraging.     

Foraging Success,Agonism, and Predator Alarms: Behavioral Predictors of Cortisol in <Emphasis Type="Italic">Lemur catta</Emphasis>

Primate social grouping is understood as an adaptive strategy for mitigating environmental selection pressures, but the relative importance of various pressures may vary. Physiological measures of well-being can show their short-term impacts and suggest their relative importance and capacity to provide ultimate or proximate control of group size. I examined correlations between pressures commonly proposed as causes of social grouping (foraging success, intergroup and intragroup agonism, and predation risk) and individual levels of fecal cortisol, a hormonal stress measure, in a free-ranging population of Lemur catta. I collected behavioral data on 45 female Lemur catta at Berenty Reserve, Madagascar, over 3 seasons (August 1999-July 2000) and determined individual cortisol levels from 474 fecal samples. Neither predator alarm rates nor intragroup agonism rates correlated with cortisol levels in any season. However, females with low daily food intake and high rates of escalated intergroup defense exhibited higher cortisol levels. The data suggest that acquisition and defense of food resources are principal challenges in Lemur catta, and may be important factors determining social grouping and other behavioral or life history adaptations.     

Measuring social tolerance: An experimental approach in two lemurid primates

Social tolerance crucially affects the life of group‐living animals as it can influence, among other things, their competitive regimes, access to food, learning behavior, and recruitment. However, social tolerance tests were mainly conducted in semi‐free or captive populations, and we know little about the behavioral mechanisms and consequences of social tolerance under natural conditions. We therefore developed a co‐feeding experiment to measure social tolerance in groups of wild and captive animals across two primate species. Specifically, we recorded the social tolerance level of redfronted lemurs (Eulemur rufifrons, four wild, one captive group) and ringtailed lemurs (Lemur catta, three wild, three captive groups) by presenting a clumped food resource in an experimental arena, and recorded patterns of resource use during the experiment. Because redfronted lemurs exhibit lower levels of decided conflicts than ringtailed lemurs, we predicted that they would be socially more tolerant. The probability for an individual to feed in the arena was higher in redfronted lemurs than in ringtailed lemurs. In addition, in both species, the probability for an individual to feed in the arena was higher in the captive populations than in their wild counterparts, suggesting that proximate factors, such as a relaxation of feeding competition in captivity, may adapt species‐specific levels of social tolerance to local levels of food availability. Hence, the number of individuals co‐feeding on a valuable food resource appears to be a useful proxy of social tolerance that could be measured with this experimental setup in other wild and captive species as well.     

A new case of fish-eating in Japanese macaques: implications for social constraints on the diffusion of feeding innovation

This is the first detailed report of social factors affecting fish-eating in Japanese macaques under natural circumstances. We video-recorded a complete event of fish eating, involving a new fish food species for the monkeys on Koshima island. Following the discovery of a large beached sea bass by a peripheral male, we observed a total of 16 individuals feeding on the fish in turns, and interacting around it. The rank order of access to the fish was mainly explained by the spatial position of group members, whereas dominance determined how long the fish was monopolized. Although limited, the tolerated presence of close-bystanders while feeding was affected by kinship and affiliation. Genealogic data suggested that fish-eating behavior was well maintained in terms of maternal lineages. This report should contribute to a better understanding of how social features may constrain the long-term diffusion of feeding innovations in free-ranging primate groups.     

Distribution of Affiliative Behavior Across Kin Classes and Their Fitness Consequences in Mandrills

Multimale–multifemale primate groups are ideal models to study the impact of kinship on the evolution of sociality. Indeed, the frequent combination of female philopatry and male reproductive skew produces social systems where both maternal and paternal kin are co‐resident. Several primates are known to bias their behavior toward both maternal and paternal kin. Moreover, allocation of affiliation toward paternal kin has been shown to depend on the availability in maternal kin: Female baboons invest more in paternal kin after the loss of preferred maternal kin. Here, we examined how affiliation co‐varies across kin classes in juvenile mandrills (Mandrillus sphinx), an Old World primate living in a multimale–multifemale society. While affiliation levels observed with the mother and with maternal half‐sibs co‐varied positively, especially in young females, we found that levels of affiliation among paternal half‐sibs correlated negatively with levels of affiliation among individuals from the same matriline (distant kin), possibly as a result of kin availability. In addition, in social species, social bonds between individuals have been linked to differentiated fitness consequences: More socially integrated individuals generally enjoy higher fitness. We therefore also tested whether affiliation during early life impacts fitness. We showed that the global amount of affiliation during juvenescence translated into possible reproductive benefits: Females who were more socially integrated gave birth on average a year before females that were less socially integrated. However, age at first reproduction was not predicted by the amount of affiliation exchanged with any particular kin class. These results add to the growing body of evidence demonstrating differential investment in bonding and possible social adjustments among different kin categories and emphasizing once more the adaptive value of sociality.     

Controversy over the application of current socioecological models to folivorous primates: Colobus vellerosus fits the predictions

We explore the applicability of the current socio-ecological model to characterize the social structure of Colobus vellerosus, a folivorous primate. The current socio-ecological model predicts that female social relationships should respond in predictable ways to food abundance and distribution and associated competitive regimes. It appears to successfully explain variation in social structure in some primate species; however, recent research indicates that several folivorous or folivore-frugivorous species seem to be exceptions. We present data on social relationships and social structure in two groups of C. vellerosus over 15 months at Boabeng-Fiema, Ghana. As predicted by the model, our results indicate the co-occurrence of 1) low levels of grooming between female C. vellerosus when compared with other species, 2) an absence of female coalitions over food, and 3) female dispersal. Taken together, these traits suggest a "Dispersal-Egalitarian" species. However, our results also indicate female-female affiliation was higher than male-female affiliation, which was more indicative of a "female resident" species. Our data also suggests inter-sexual affiliation varied among groups. This variation in inter-sexual affiliation could be due to variation in the intensity of infanticidal threats between groups. The combination of these social characteristics lead us to conclude that C. vellerosus' social structure is largely congruent with the ecological indicators of food distribution and female competitive regime that we have previously documented, which indicated high quality foods were not monopolizable or usurpable and behavioral evidence of within-group contest competition (i.e. supplantations over food) was rare. But the combination of higher female-female affiliation (compared to male-female) and female dispersal is difficult to explain in light of predictions, unless future work reveals female residency is more predominant than female dispersal in our population. We also discuss reasons why some folivores do not appear to fit the predictions of the current socio-ecological model.     

Kinship and similarity in residency status structure female social networks in black‐and‐white colobus monkeys (colobus vellerosus)

Kinship shapes female social networks in many primate populations in which females remain in their natal group to breed. In contrast, it is unclear to which extent kinship affects the social networks in populations with female dispersal. Female Colobus vellerosus show routine facultative dispersal (i.e., some females remain philopatric and others disperse). This dispersal pattern allowed us to evaluate if facultative dispersed females form social networks shaped by an attraction to kin, to social partners with a high resource holding potential, or to similar social partners in terms of maturational stage, dominance rank, and residency status. During 2008 and 2009, we collected behavioral data via focal and ad libitum sampling of 61 females residing in eight groups at Boabeng‐Fiema, Ghana. We determined kinship based on partial pedigrees and genotypes at 17 short tandem repeat loci. Kinship influenced coalition and affiliation networks in three groups consisting of long‐term resident females with access to a relatively high number of female kin. In contrast, similar residency status was more important than kinship in structuring the affiliation network in one of two groups that contained recent female immigrants. In populations with female dispersal, the occurrence of kin structured social networks may not only depend on the kin composition of groups but also on how long the female kin have resided together. We found no consistent support for females biasing affiliation toward partners with high resource holding potential, possibly due to low levels of contest competition and small inter‐individual differences in resource holding potential. Am J Phys Anthropol 153:365–376, 2014. © 2013 Wiley Periodicals, Inc.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

A preliminary study of kinship and social organization in a semi-free-ranging group ofLemur catta

From long-term studies of a number of anthropoid species, many investigators have shown that kinship affinities affect social relationships. Factors such as proximity, social grooming, dominance rank, and mating patterns have been shown to be related to kinship. In this paper, we report the results of a preliminary study of the social organization of a group of prosimians (Lemur catta) in which individuals were identified and kinship affinities were known. We found that close matrilineal kin preferred to groom one another and to remain in close proximity more than did nonkin and distantly related animals. Furthermore, no copulations were observed within matrilines. These results are similar to those found in a number of species of anthropoids. This research was conducted on a semi-free-ranging group at the Duke University Primate Facility, Durham, North Carolina.     

Reconciliation and third‐party affiliation in carrion crows

Conflicts are costly because they can damage social relationships. To buffer conflicts, various species use post‐conflict behaviour, such as reconciliation or third‐party affiliation. Both behaviours have predominantly been studied in non‐human primates. However, recently, studies revealed post‐conflict behaviour in other mammalian and some bird species (e.g., corvids). While third‐party affiliation has been reported in several corvid species, reconciliation has only rarely been observed. The social structure of the studied groups has been postulated as a reason for the absence of reconciliation. Here, we investigated whether post‐conflict behaviours in corvids indeed mirror the relationship structure. We studied the behaviour of a newly established group of juvenile carrion crows (Corvus corone corone), where pair bonds had not yet been established. We applied a combination of observations and food monopolisation experiments to quantify the use of post‐conflict behaviours. Provisioning food in one or two pieces induced different patterns of aggression during feeding and differently affected the affiliation patterns after feeding. Specifically, victims of severe aggression affiliated with third parties after conflicts in the two‐piece condition, while aggressors affiliated with victims of mild aggression in the one‐piece condition. We thus provide the first evidence that a corvid species, crows, flexibly engage in both third‐party affiliation and reconciliation.     

Conflict and reconciliation behavior trends of the bottlenose dolphin (Tursiops truncatus)

Wild bottlenose dolphin (Tursiops truncatus) populations display societal structures characterized by numerous and frequent changes in group composition, complex social relationships, and high levels of cooperation, attributes also observed in human and nonhuman primate cultures. Maintaining social relationships under such elemental conditions can frequently create conflict—and the opportunity for reconciliation—among group members. The conflict and reconciliation behavior patterns of the chimpanzee (Pan troglodytes) have been studied extensively; trends are well‐documented in the wild and in captivity. Apparent cultural similarities have prompted several analogous studies on wild and captive bottlenose dolphins. This research attempted to corroborate previous efforts by analyzing the social behavior of seven captive bottlenose dolphins to determine the effects of sex and age on the frequency of conflict and reconciliation, and to investigate the incidence of consolatory behavior within the group. A total of 3,428 interactions involving focal animals, 414 of which were conflict episodes, were documented during 261 hr of videotaped observations. Although the sample size precluded meaningful statistical evaluation of the influence of sex on conflict and reconciliation, participant age was a significant determinant of conflict frequency. Conversely, age did not impact frequency of reconciliation, which only occurred after 18% of all conflict interactions. Little to no definitive evidence of consolation was apparent within the study group. While results partially support the findings of previous dolphin reconciliation research, extensive behavioral studies of wild populations should be conducted before generating broad comparisons between human terms and nonhuman behavioral interactions. Zoo Biol 29:567–585, 2010. © 2009 Wiley‐Liss, Inc.     

Social effects on foraging behavior and success depend on local environmental conditions

In social groups, individuals' dominance rank, social bonds, and kinship with other group members have been shown to influence their foraging behavior. However, there is growing evidence that the particular effects of these social traits may also depend on local environmental conditions. We investigated this by comparing the foraging behavior of wild chacma baboons, Papio ursinus, under natural conditions and in a field experiment where food was spatially clumped. Data were collected from 55 animals across two troops over a 5‐month period, including over 900 agonistic foraging interactions and over 600 food patch visits in each condition. In both conditions, low‐ranked individuals received more agonism, but this only translated into reduced foraging performances for low‐ranked individuals in the high‐competition experimental conditions. Our results suggest one possible reason for this pattern may be low‐ranked individuals strategically investing social effort to negotiate foraging tolerance, but the rank‐offsetting effect of this investment being overwhelmed in the higher‐competition experimental environment. Our results also suggest that individuals may use imbalances in their social bonds to negotiate tolerance from others under a wider range of environmental conditions, but utilize the overall strength of their social bonds in more extreme environments where feeding competition is more intense. These findings highlight that behavioral tactics such as the strategic investment of social effort may allow foragers to mitigate the costs of low rank, but that the effectiveness of these tactics is likely to be limited in certain environments.     

Habitat Use and Activity Patterns as an Indication of Fragment Quality in a Strepsirrhine Primate

Considerable intraspecific variation exists in responses to habitat fragmentation owing to regional differences in fragment quality. Habitat use and activity patterns of resident populations are related to the abundance and predictability of resources in time and space, and thus space use is one of the most important considerations for evaluating habitat quality. Here I examine inter- and intrasite differences in the ranging behavior; use of the matrix, i.e., surrounding nonhabitat; and activity budgets of ring-tailed lemurs (Lemur catta) inhabiting two forest fragments—Anja Special Reserve and Tsaranoro Valley Sacred Forest—in Madagascar’s central highlands to test the prediction that intraspecific variation in habitat use and activity patterns is indicative of fragment quality. At Anja, Lemur catta has access to abundant year-round anthropogenic resources (introduced fruit trees, agricultural crops, water), whereas the population at Tsaranoro relies on seasonally variable and patchily distributed resources throughout the forest and matrix. Lemur catta at Anja occupy smaller home ranges; have shorter daily path lengths (DPLs); and spend less time foraging and more time resting, locomoting, and engaging in social and territorial behavior. In contrast, groups at Tsaranoro occupy larger home ranges, have longer DPLs, rely heavily on the matrix, and expend most of their energy in foraging behavior. These differences point to variation in the relative habitat quality of the two fragments and are thus an important consideration for conservation managers when assessing the capacity of forest fragments to sustain populations.     

Daily activity and light exposure levels for five species of lemurs at the duke lemur center

Light is the primary synchronizer of all biological rhythms, yet little is known about the role of the 24‐hour luminous environment on nonhuman primate circadian patterns, making it difficult to understand the photic niche of the ancestral primate. Here we present the first data on proximate light–dark exposure and activity–rest patterns in free‐ranging nonhuman primates. Four individuals each of five species of lemurs at the Duke Lemur Center (Eulemur mongoz, Lemur catta, Propithecus coquereli, Varecia rubra, and Varecia variegata variegata) were fitted with a Daysimeter‐D pendant that contained light and accelerometer sensors. Our results reveal common as well as species‐specific light exposure and behavior patterns. As expected, all five species were more active between sunrise and sunset. All five species demonstrated an anticipatory increase in their pre‐sunrise activity that peaked at sunrise with all but V. rubra showing a reduction within an hour. All five species reduced activity during mid‐day. Four of the five stayed active after sunset, but P. coquereli began reducing their activity about 2 hours before sunset. Other subtle differences in the recorded light exposure and activity patterns suggest species‐specific photic niches and behaviors. The eventual application of the Daysimeter‐D in the wild may help to better understand the adaptive evolution of ancestral primates. Am J Phys Anthropol 153:68–77, 2014. © 2013 Wiley Periodicals, Inc.     

Beiträge zur: Anthropologie,ethnographie und sprachforschung der kashuiéna indianer sowie akkulturationserscheinungen

Studies of Dravidian kinship have neglected the importance of the cross‐sibling relationship. A comparative analysis of data gathered in a Sri Lankan Muslim community shows: (1) normative depictions of cross‐sibling relationships do not reflect or explain actual behavior patterns; and (2) variation in post‐marital cross‐sibling relationships is largely accounted for by the presence or absence and use of the dowry. The overarching purpose is to show that any comprehensive analysis of the Dravidian kinship system must include an analysis of cross‐sibling relationships and dowry practices.     

Social Network Influences Decision Making During Collective Movements in Brown Lemurs (<Emphasis Type="Italic">Eulemur fulvus fulvus</Emphasis>)

Many animal species live as a group and must therefore move as such. Several authors have suggested that the mechanisms underlying collective movements in primate species appear to rely on complex cognitive skills, given their high level of cognitive abilities. However, recent studies have highlighted the fact that complex patterns do not necessarily imply complex mechanisms. We used a modeling approach to investigate the patterns of collective movement in a semi-free-ranging group of brown lemurs. We recorded via digital video cameras the order and joining latencies of the 11 individuals of the group during the departure time of spontaneous group movements. We then assessed whether mimetic mechanisms or the existence of a leader were underlying conditions for the joining process by testing 5 computer models relying respectively on 5 hypotheses: the independence of individuals, an anonymous mimetism, a mimetism according to kinship, a mimetism according to affiliation, and eventually the existence of a leader. We found that departure latencies, associations, and the order of individuals at departure time could all be explained by the mimetism according to affiliation model. Thus, an individual’s decision to join the collective movement or not depended on the decision taken by its preferred social partners. These results show the importance of social parameters in primate decision making and that the high cohesion displayed by the group members might not be constrained merely by ecological factors such as predation or foraging consideration.     

A QUANTITATIVE ASSESSMENT OF DOMINANCE RELATIONS AMONG BOTTLENOSE DOLPHINS

Agonistic behavior of bottlenose dolphins was studied at Brookfield Zoo for nearly 4.5 yr, and dominance relationships were determined using a quantitative technique adapted from primate behavioral research. Dominance relations among dolphins were influenced by the gender of participants. Male dolphins were clearly and consistently dominant to females, and intersexual agonism occurred at moderate rates with seasonal peaks in spring and fall. Dominance relationships among female dolphins were age-ordered and stable, even though agonism among females did occur at uniformly low rates. In contrast, the two males had a changeable dominance relationship in which periods of stability and low-level agonism were interspersed with episodes of intense competition. Zoo-based research revealed patterns of behavior that conformed to current knowledge about bottlenose dolphin social structure. Moreover, research in a zoo setting facilitated development of a quantitative technique that can be used to assess cetacean dominance relationships in field research.