Female Coordination of Group Travel in Wild Propithecus and Eulemur

Coordination of primate group movements by individual group members is generally categorized as leadership behavior, which entails several steps: deciding where to move next, initiating travel, and leading a group between food, water sources, and rest sites. Presumably, leaders are able to influence their daily foraging efficiency and nutritional intake, which could influence an individual's feeding ecology and long-term reproductive success. Within anthropoid species, females lead group movements in most female-bonded groups, while males lead groups in most nonfemale-bonded groups. Group leadership has not been described for social prosimians, which are typically not female-bonded. We describe group movements in two nonfemale-bonded, lemurid species living in southeastern Madagascar, Propithecus diadema edwardsi and Eulemur fulvus rufus. Although several social lemurids exhibit female dominance Eulemur fulvus rufus does not, and evidence for female dominance is equivocal in Propithecus diadema edwardsi. Given the ecological stresses that females face during reproduction, we predict that females in these two species will implement alternative behavioral strategies such as group leadership in conjunction with, or in the absence of, dominance interactions to improve access to food. We found that females in both species initiated and led group movements significantly more often than males did. In groups with multiple females, one female was primarily responsible for initiating and leading group movements. We conclude that female nutritional needs may determine ranging behavior to a large extent in these prosimian species, at least during months of gestation and lactation.     

Life history of Eulemur fulvus rufus from 1988-1998 in southeastern Madagascar

In this study, we compare the life-history patterns of male and female Eulemur fulvus rufus based on longitudinal data collected on individuals from two study groups from 1988-1998 in southeastern Madagascar. Mean group size was 9.5 individuals, and groups either contained more adult males than females or equal numbers of both sexes. Females reproduced for the first time between 2 and 4 years of age and reproduced each year, although the mean interbirth interval between surviving offspring was 2.1 years. An average of two adult females reproduced annually in each social group, and age and body weight may positively influence reproductive success. Females also appear to be philopatric but not female-bonded. Young natal males immigrated between 3 and 4.5 years of age and may join a new group within 612 months based on the age of emigrants. Once in a social group, they remained until old age, although a male's spatial position in the social group varied with age. Young nonnatal males were members of the social core and had the first opportunity to mate with all estrous females. Older males were peripheral to the social group and mated with females later in their cycle. We hypothesize that group size, the number of females in the group, and individual variation in reproductive success is influenced by several ecological conditions at this site: extreme variability in food availability during reproductive periods, the lack of large food patches, low plant species diversity, and small numbers of important aseasonal food sources such as Ficus species.     

Social thermoregulation in redfronted lemurs (Eulemur fulvus rufus)

Pronounced seasonality, with temperatures dropping as low as 5 degrees C during the dry season, has led to the hypothesis that Malagasy lemurs face cold stress and respond to this by inactivity and social thermoregulation, i.e. resting in tight body contact with conspecifics. Compared to anthropoids, lemur groups are comprised of an unusually high number of males, leading to an even or slightly male-biased adult sex ratio. According to one hypothesis, females may benefit from these surplus males in their groups if males huddle with females. The results of this study on redfronted lemurs (Eulemur fulvus rufus) in Kirindy Forest, Madagascar revealed that the animals indeed responded to cold ambient temperatures by increased inactivity and the formation of huddling groups. However, surplus males did not participate more frequently than expected in huddling groups with females and females do not, therefore, benefit from the high number of males in their groups by increased social thermoregulation.     

Distributed leadership in semifree-ranging white-faced capuchin monkeys

We investigated the initiation of group movements in white-faced capuchin monkeys, Cebus capucinus, with the aim of determining whether a single individual with high dominance status consistently leads movements or whether leadership is distributed between group members. The group studied was reared in semifree-ranging conditions. A multivariate analysis followed by univariate analyses demonstrated that leadership was not concentrated on a single individual in this species. All individuals could initiate a collective movement. Nearly half of group members regularly succeeded in recruiting at least three followers. Although both sexes had similar rates of start attempts, females succeeded more frequently than males. We found no significant effect of the dominance status on the percentage of successful attempts. The use of a slow speed, looking back towards the other group members, or trills by the initiator heightened the likelihood of success in group movement initiation. An initiator starting from a core position in a clumped group was more successful than one starting from an edge position in a clumped group or from a dispersed group. Furthermore, the probability of successful start attempts was higher when the group remained stationary for a long period. Leadership in white-faced capuchins appears to be distributed between group members rather than exclusively concentrated on high-ranking individuals. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.      

Marking behaviour in two lemur species (L. fulvus and L. macaco): relation to social status, reproduction, aggression and environmental change.

The influence of social status, reproductive and agonistic contexts and environmental change on scent-marking and allomarking rates were studied in captive groups of Lemur fulvus and Lemur macaco. No evidence of female social dominance over males appeared in either species. In L. fulvus, intrasexual relationships were characterized by the dominance of one adult male over another and by the existence of female affiliative association ('central' vs. 'peripheral' females). In L. macaco, no intrasexual dominance relationships were apparent except for a brief ostracism of one female. In both species, (1) intrasexual differences in social status were related to differences in marking rates, (2) no direct relation appeared between marking rates and aggression or reproduction, (3) allomarking was not differentially directed towards specific individuals and (4) physical environmental factors clearly influenced scent-marking and allomarking rates. These results are discussed in relation to the possible functions of marking behaviour in intragroup relations.     

Ecological correlates to activity and habitat use of two prosimian primates: Eulemur rubriventer and Eulemur fulvus rufus in Madagascar

In this paper, I provide data on the possible effects of group size and seasonal changes in food availability on the activity and habitat use patterns of two species of prosimian primate: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). General and subtle seasonal differences were observed between lemur species in (1) group size and composition, (2) activity profiles, and (3) habitat use. Rufous lemur groups were larger (mean = 8 individuals) and contained more adults than red-bellied lemur groups (mean = 3 individuals). The overall degree and distribution of diurnal activity differed between lemur species and varied within species with seasonal changes in food availability. In general, rufous lemurs traveled more often than red-bellied lemurs. During food scarcity, both species increased the amount of time spent feeding, although peak feeding and traveling times differed. Both species also preferred horizontal substrates; however, during food scarcity, red-bellied lemurs used terminal branches more often while feeding than rufous lemurs. In addition, red-bellied lemurs used the lower middle story forest and rested in taller, upper canopy trees more often than rufous lemurs. Differences in activity and habitat use patterns between lemur species were more related to seasonal changes in food availability than overall differences in group size. These behavioral patterns may represent different strategies used by each lemur species to avoid directly competing for similar resources during times of food scarcity. © 1996 Wiley-Liss, Inc.     

Coordination of Group Movements in Wild Red-fronted Lemurs (<Emphasis Type="Italic">Eulemur rufifrons</Emphasis>): Processes and Influence of Ecological and Reproductive Seasonality

Group-living species have to coordinate collective actions to maintain cohesion. In primates, spatial movements represent a meaningful model to study group coordination processes across different socio-ecological contexts. We studied 4 groups of red-fronted lemurs (Eulemur rufifrons) in Kirindy Forest, Madagascar, between 2008 and 2010 across different ecological and reproductive seasons. We collected data on ranging patterns using GPS collars and observational data on different predefined parameters of group movements, including initiation, leadership, followership, overtaking events, termination, and travel distances. Cohesion of these relatively small, egalitarian lemur groups was high year-round, but daily path length and home range size varied considerably between ecological seasons, presumably due to long-distance migrations of some groups at the beginning of the rainy season. Individuals of different age and sex classes successfully initiated group movements. However, stable female leadership prevailed year-round, irrespective of ecological and reproductive season, which might be due to higher or more specific energetic requirements of reproduction. In contrast to lemur species with a more despotic social structure, female red-fronted lemurs did not recruit more followers than males. Adult leaders recruited more followers than subadult ones. Further, recruitment success was higher during the peak of the dry season, when predation risk appeared to be higher. Distances of single group movements did not depend on the initiator’s sex and age or on ecological seasons. Our results provide new insights into seasonal variability of coordination processes and the role of social dominance in lemur group movements, thereby contributing to a comparative perspective from a primate radiation that evolved group living independently of anthropoids.     

Aggressive and neutral interventions in conflicts in captive groups of brown lemurs (Eulemur fulvus fulvus)

Third-party interventions in conflicts have revealed complexity in primate social relationships. This type of intervention has seldom been analyzed in prosimians, although many of these species exhibit complex (multimale/multifemale) social organizations. The present study on captive brown lemurs (Eulemur fulvus fulvus) shows that dominant individuals were more likely to intervene in conflicts. Both males and females intervened aggressively in conflicts. Female aggressive interventions occurred mainly on behalf of close kin, whereas males mainly intervened on behalf of juveniles. This study also provides the first record of neutral or peaceful interventions in lemurs. Although females intervened neutrally, almost all neutral interventions were by dominant males. Dominant males intervened in conflicts neutrally more often than aggressively, principally in conflicts between adults and juveniles or between juveniles. Neutral interventions by males always ended the conflicts and were often followed by affiliative contacts between participants (intervenors and opponents). In lemurs, female interventions can be explained by kin selection, while the nature of dominant males' interventions suggests a control role. Interventions by males on behalf of juveniles may increase the formers' fitness.     

How can leadership processes in European bison be used to improve the management of free-roaming herds

For several years, several wild species are experiencing a comeback in Europe, especially large herbivores. Despite the good news, the increased number of wild herbivores also potentially increases human-wildlife conflicts due to crop damages and road traffic accidents where such species have been involved in previously. In this context, studying the movements of animal groups is particularly relevant for managing their use of space and ensure sufficient cohabitation with human populations. We thus studied the European bison (Bison bonasus), a species concerned in several rewilding programs, to understand to what extent individual characteristics and social relationships are involved in the leadership process and how these factors influence the success of group movements. We observed a herd of 14 individuals in Zuid-Kennemerland National Park (the Netherlands) and analysed the initiation phase of spontaneous group movements. We showed that leadership was distributed throughout the group but the two oldest females showed higher propensity to initiate and to be followed. They seemed to have a high social power and a strong capacity to federate probably due to their dominance rank and their knowledge of the areas. The joining process was faster when animals were grouped before departure and when the initiator moved in the direction towards which the majority of individuals was oriented. Individuals joined the movement according to a selective mimetic process, based on kinship. These results, combined with virtual fence device, could be used to manage herd movements in a given territory and thus, might be an innovative tool to decrease human-wildlife conflicts.     

Leading ladies: leadership of group movements in a pair-living, co-dominant, monomorphic primate across reproductive stages and fruit availability seasons

For gregarious species, individuals must maintain cohesion while minimizing the costs of coordinated travel. Leaders of group movements potentially influence energy expenditure, energy intake, and predation risk for individuals in the group, which can have important fitness consequences. Models of pair-living species predict that energetic asymmetries lead to an emergent leader, with those in greater need leading. We investigated sex differences in leadership in pairs of red-bellied lemurs, Eulemur rubriventer, a monomorphic species with bisexual dispersal and no discernible hierarchy, to determine whether higher energetic requirements by adult females lead to female leadership. We collected leadership data in Ranomafana National Park, Madagascar on six groups of habituated E. rubriventer for 13 consecutive months between 2004-2005. To determine whether females led group movements more than males, we examined the difference in leadership frequencies of progressions in adult males and adult females within each group (n = 1,346 progressions). We further investigated the behavioral context (i.e. travel followed by feeding or not) and seasonal contexts (fruit availability, reproduction) of leadership. Group leadership was distributed, with different individuals leading the group at different times. However, females led significantly more than males, a pattern which was consistent in both feeding and non-feeding contexts and throughout all fruiting seasons and reproductive stages. While disparities in energetic status among the sexes may impact leadership in this species, leadership did not differ with changes in food availability or reproductive stage, and thus we were unable to determine whether female leadership might be related to changes in energetic status. Females may have higher energetic needs than males at all times, not merely seasonally, or female leadership may be unrelated to immediate energetic need. Rather, female leadership may be a legacy of female dominance not currently expressed in other contexts.     

Self-Organization in Primates: Understanding the Rules Underlying Collective Movements

Patterns of collective movements, such as the distribution of leadership and the organization of individuals, may be either homogeneously (no leader, no specific order), or heterogeneously (1 or several leaders, and a highly stable order) distributed. Members of a group need to synchronize their activities and coordinate their movements, despite the fact that they differ in physiological or morphological traits. The degree of difference in these traits may affect their decision-making strategy. We demonstrate how a theoretical model based on a variation of a simple mimetic rule, i.e., an amplification process, can result in each of the various collective movement patterns and decision-making strategies observed in primates and other species. We consider cases in which 1) the needs of different individuals are identical and social relationships are equivalent between group members, 2) the needs of individuals are different and social relationships are equivalent, and 3) the needs of individuals are different and social relationships are different. Finally, 4) we assess how the synergy between 2 mimetism rules, specifically the probability of joining a movement and that of canceling an initiation, allows group members to stay synchronized and cohesive. Our models suggest that similar self-organized processes have been selected as reliable and well-adapted means for optimal collective decisions across species, despite differences in their biological and social characteristics.     

Amino acid sequences of the alpha and beta chains of adult hemoglobin of the brown lemur, Lemur fulvus fulvus.

Globin prepared from hemoglobin of the brown lemur (Lemur fulvus fulvus) was separated into alpha and beta chains by chromatography on a CM 52 column. The S-aminoethylated alpha and beta chains were each digested with trypsin and resulting peptides were isolated. The amino acid sequences of the tryptic peptides were established. The ordering of these peptides in the alpha and beta chains was deduced from the homology of their amino acid sequences with that of human adult hemoglobin. The primary structure of brown lemur hemoglobin thus obtained differs from that of human hemoglobin in 15 amino acids in the alpha chain and 26 in the beta chain.     

Decision-making processes: The case of collective movements

Besides focusing on the adaptive significance of collective movements, it is crucial to study the mechanisms and dynamics of decision-making processes at the individual level underlying the higher-scale collective movements. It is now commonly admitted that collective decisions emerge from interactions between individuals, but how individual decisions are taken, i.e. how far they are modulated by the behaviour of other group members, is an under-investigated question. Classically, collective movements are viewed as the outcome of one individual's initiation (the leader) for departure, by which all or some of the other group members abide. Individuals assuming leadership have often been considered to hold a specific social status. This hierarchical or centralized control model has been challenged by recent theoretical and experimental findings, suggesting that leadership can be more distributed. Moreover, self-organized processes can account for collective movements in many different species, even in those that are characterized by high cognitive complexity. In this review, we point out that decision-making for moving collectively can be reached by a combination of different rules, i.e. individualized (based on inter-individual differences in physiology, energetic state, social status, etc.) and self-organized (based on simple response) ones for any species, context and group size.     

Social Structure Affects Initiations of Group Movements but Not Recruitment Success in Japanese Macaques (<Emphasis Type="Italic">Macaca fuscata</Emphasis>)

Research on collective movements has often focused on the sociodemographic parameters explaining the success of some individuals as leaders or initiators of collective movements. Several of these studies have shown the influence of social structure, through kinship and affiliative relationships, on the organization of collective movements. However, these studies have been conducted on semi-free-ranging groups of macaques that were not faced with a natural environment and its constraints. In the socially intolerant rhesus macaque (Macaca mulatta) the success of an initiator correlates with its hierarchical rank, the most dominant individuals being the most successful. We investigated the collective movements of another socially intolerant macaque species, Japanese macaques, in the wild, to assess whether the social structure was still a determinant factor under natural conditions. In line with previous studies of macaques, we found that social structure drove the organization of collective movements. More dominant individuals initiated more collective movements. However, dominance did not affect the success of an initiation, i.e., the number of individuals joining. In addition, kinship strongly constrained the associations observed in females during collective movements. These results reflect the social structure of Japanese macaques, in which strong power asymmetry and kinship relationships constrain the majority of interactions between individuals within the group. Moreover, these results are similar to those observed in semi-free-ranging rhesus macaques and support the hypothesis of an effect of social determinants on collective movements of primates even under natural conditions.     

Ecological correlates to social structure in two lemur species in Madagascar

In this study, I tested two hypotheses regarding the relationship of ecological variables (size, density, and distribution of patches) and infant developmental patterns to lemur social structure using two prosimian primates in Ranomafana, Madagascar: the rufous lemur (Eulemur fulvus rufus) and the red-bellied lemur (Eulemur rubriventer). Three predictions regarding the general effects of patch size and subgroup size on lemur feeding rates were supported: (1) Rufous lemurs used large patches; red-bellied lemurs used smaller patches; (2) larger subgroups of rufous lemurs used larger patches; and (3) rufous lemur feeding rates decreased significantly with increases in subgroup size and patch size, whereas size and patch size had no significant effect on red-bellied lemur feeding rates. However, food item size (fruit) had a more significant effect on rufous and red-bellied lemur feeding rates than either patch size or subgroup size. When similar-sized fruits were compared, rufous lemur feeding rates on small fruit were most affected by patch size, yet feeding rates on medium-sized fruit were most affected by subgroup size. Neither lemur species used patches in consistent ways seasonally. During periods of food abundance, rufous lemurs used many small, common, and clumped patches. In food scarcity periods, they used fewer, larger, rarer, and less clumped patches; groups migrated when food became most scarce. Red-bellied lemurs also used patches in variable ways, but these patterns were not linked with food availability. Finally, infant development patterns differed between lemur species; red-bellied lemur males cared for offspring and infants reached developmental landmarks faster than rufous lemur infants. Therefore, red-bellied lemur group size may be constrained by the need for additional infant care by other group members. In contrast, rufous lemur group size may be constrained by patch availability during the most critical period of food scarcity. © 1996 Wiley-Liss, Inc.     

Collective decision-making in white-faced capuchin monkeys

In group-living animals, collective movements are a widespread phenomenon and occur through consensus decision. When one animal proposes a direction for group movement, the others decide to follow or not and hence take part in the decision-making process. This paper examines the temporal spread of individual responses after the departure of a first individual (the initiator) in a semi-free ranging group of white-faced capuchins (Cebus capucinus). We analysed 294 start attempts, 111 succeeding and 183 failing. Using a modelling approach, we have demonstrated that consensus decision-making for group movements is based on two complementary phenomena in this species: firstly, the joining together of group members thanks to a mimetic process; and secondly, a modulation of this phenomenon through the propensity of the initiator to give up (i.e. cancellation rate). This cancellation rate seems to be directly dependent upon the number of followers: the greater this number is, the lower the cancellation rate is seen to be. The coupling between joining and cancellation rates leads to a quorum: when three individuals join the initiator, the group collectively moves. If the initiator abandons the movement, this influences the joining behaviour of the other group members, which in return influences the initiator''s behaviour. This study demonstrates the synergy between the initiator''s behaviour and the self-organized mechanisms underlying group movements.     

Sex differences in leadership during group movement in mantled howler monkeys (Alouatta palliata)

Benefits of group life depend in large part on whether animals remain cohesive, which often requires collective decisions about where and when to move. During a group movement, the leader may be considered as the individual occupying the vanguard position of the group progression, when its movement evokes following by other group members. In nondespotic societies, individuals with greater incentives to move frequently are leaders. During 15 months of observations (1,712 contact hours), we investigated two mantled howler monkey (Alouatta palliata) groups at La Flor de Catemaco (Los Tuxtlas, Mexico) to examine whether sex and female reproductive state influenced leadership likelihood in two contexts: movements toward feeding trees; movements associated with loud calls, a group-defense behavior used by males of this genus. Females led and occupied forward positions during group movements toward feeding trees more often than adult males. Adult females led these movements more frequently when they were gestating than when they were lactating or cycling. There were no differences between sexes in the leadership of group movements associated with loud calls. Leadership by gestating females is perhaps the result of their higher nutritional/energetic needs when compared with cycling females, and of their greater mobility when compared with lactating females carrying dependent offspring. Female leadership during movements toward feeding trees may be a mechanism to optimize access to food resources in mantled howler monkeys.     

Consistency of leadership in shoals of mosquitofish (Gambusia holbrooki) in novel and in familiar environments

In social animal groups, an individual's spatial position is a major determinant of both predation risk and foraging rewards. Additionally, the occupation of positions in the front of moving groups is generally assumed to correlate with the initiation of group movements. However, whether some individuals are predisposed to consistently occupy certain positions and, in some instances, to consistently lead groups over time is as yet unresolved in many species. Using the mosquitofish (Gambusia holbrooki), we examined the consistency of individuals' spatial positions within a moving group over successive trials. We found that certain individuals consistently occupied front positions in moving groups and also that it was typically these individuals that initiated group decisions. The number of individuals involved in leading the group varied according to the amount of information held by group members, with a greater number of changes in leadership in a novel compared to a relatively familiar environment. Finally, our results show that the occupation of lead positions in moving groups was not explained by characteristics such as dominance, size or sex, suggesting that certain individuals are predisposed to leadership roles. This suggests that being a leader or a follower may to some extent be an intrinsic property of the individual.     

The Organization of Collective Group Movements in Wild Barbary Macaques (Macaca sylvanus): Social Structure Drives Processes of Group Coordination in Macaques

Social animals have to coordinate activities and collective movements to benefit from the advantages of group living. Animals in large groups maintain cohesion by self-organization processes whereas in smaller groups consensus decisions can be reached. Where consensus decisions are relevant leadership may emerge. Variation in the organization of collective movements has been linked to variation in female social tolerance among macaque species ranging from despotic to egalitarian. Here we investigated the processes underlying group movements in a wild macaque species characterized by a degree of social tolerance intermediate to previously studied congeneric species. We focused on processes before, during and after the departure of the first individual. To this end, we observed one group of wild Barbary macaques (Macaca sylvanus) in the Middle Atlas, Morocco using all-occurrence behaviour sampling of 199 collective movements. We found that initiators of a collective movement usually chose the direction in which more individuals displayed pre-departure behavior. Dominant individuals contributed to group movements more than subordinates, especially juveniles, measured as frequencies of successful initiations and pre-departure behaviour. Joining was determined by affiliative relationships and the number of individuals that already joined the movement (mimetism). Thus, in our study group partially shared consensus decisions mediated by selective mimetism seemed to be prevalent, overall supporting the suggestion that a species’ social style affects the organization of group movements. As only the most tolerant species show equally shared consensus decisions whereas in others the decision is partially shared with a bias to dominant individuals the type of consensus decisions seems to follow a stepwise relation. Joining order may also follow a stepwise, however opposite, relationship, because dominance only determined joining in highly despotic, but not in intermediate and tolerant species.