Male dispersal patterns in white-faced capuchins, Cebus capucinus: Part 1: patterns and causes of natal emigration

This is the first of two papers examining male dispersal patterns in white-faced capuchins. Our study was based on behavioural and demographic data collected on multiple groups of white-faced capuchins in Santa Rosa National Park, Costa Rica since 1985. Here we examine the patterns and proximate causation of male natal dispersal. Natal dispersal in white-faced capuchins occurred at a median age of 4.5 years, with no males remaining in the natal group past 8 years. Initial departure from the natal group appeared to be in response to an attraction to extragroup males and dispersing groupmates. Rates of parallel dispersal (dispersal with co-resident males and/or into groups containing familiar males) were very high for natal males (71-82%), and this pattern of dispersal may have evolved to increase inclusive fitness benefits in male-dispersed species. Additionally, this pattern of dispersal probably increases survivorship among dispersing males who are not yet physically mature, as is common in white-faced capuchins.     

Male dispersal in a provisioned multilevel group of Rhinopithecus roxellana in Shennongjia Nature Reserve, China

Most Old World monkeys show male-biased dispersal. We present the first systematic data on male dispersal in a provisioned multilevel group of Rhinopithecus roxellana, based on 4.5 years of field observations in Shennongjia National Nature Reserve, China. We evaluated both ultimate (inbreeding avoidance and male mating competition) and proximate (food availability and predation risk) factors influencing male dispersal. The focal group contained 34-53 individuals, in 3-4 one-male units (OMUs) and 1 all-male unit (AMU). We observed 37 dispersal events involving 10 of 11 adults, 7 of 8 subadults, and 7 of 15 juveniles. Most interunit transfers within the focal group occurred around the months of mating season. Adult males competed for the leader positions of OMUs mainly through aggressive takeovers, and young males transferred from the OMUs to the AMU at the median age of 41 months, forced out by leader males. No young males older than 4 years remained in natal or non-natal OMUs. The male mating competition hypothesis was supported. The young males emigrated voluntarily from the focal group at the average age of 58.6 months, and no young emigrating male was observed to return, suggesting inbreeding avoidance also played a role in the dispersal of young males. Most emigration/immigration events were parallel dispersal and occurred during intergroup encounters, suggesting increased predation risk during the dispersal period. Males were more likely to emigrate/immigrate during the months when preferred foods were most available. We compared the dispersal patterns in R. roxellana with those in gelada baboons and hamadryas baboons, both living in multilevel societies. Similar to R. roxellana, young male geladas disperse at puberty, but they may return and breed in their natal groups. Males in hamadryas also disperse, but much less commonly than in R. roxellana. Provisioning may have influenced results, and confirming studies on unprovisioned groups would be valuable.     

Unraveling the dispersal patterns and the social drivers of natal emigration of a cooperative breeding mammal,the golden lion tamarin

The study of the social drivers of animal dispersal is key to understanding the evolution of social systems. Among the social drivers of natal emigration, the conspecific attraction, aggressive eviction, and reduced social integration hypotheses predict that sexually mature individuals who receive more aggressive behavior and are engaged in less affiliative interactions are more likely to disperse. Few reports have explored these proximate factors affecting emigration in cooperatively breeding species, particularly of Neotropical primates. In this study, we investigated the dispersal patterns and tested the social drivers of natal emigration in the golden lion tamarin (Leontopithecus rosalia) — an endangered species inhabiting Atlantic rainforests fragments in Brazil. We used behavioral and demographic data collected during 7 years from 68 groups of tamarins inhabiting 20 forest fragments. Our analyses from the 160 dispersing individuals showed that dispersal success is higher for males and for those engaged in parallel dispersal, but that males and females use different strategies to enhance their dispersal success, males immigrate into established groups while females form new groups. We did not find high levels of agonistic behavior among group members before natal emigration. Instead we found that conspecific attraction drives natal emigration in both sexes, while additionally the low level of affiliative interactions within the natal group triggers male emigration. We discuss natal emigration in the broader perspective of the cooperative breeding system and the implications of these findings for the conservation of the species.     

Male Migration in Barbary Macaques (Macaca sylvanus) at Affenberg Salem

We analyzed male migration during a 20-year period in the free-ranging Barbary macaque population of Affenberg Salem. Most natal migrations occurred around puberty, but only one third of all males left the natal group. Secondary group transfers were rare. All males immediately transferred to other bisexual groups. Migration rates were highest during periods with high adult female/male ratios within social groups. Immigrants highly preferred groups with fewer males of their own age than in the natal group, and many males immigrated into groups that had no male their own age. These groups originated from a skewed distribution of resident males during group fissions. A comparison of emigrants with their natal peers supports the inbreeding avoidance hypothesis as cause of emigration rather than the male competition avoidance hypothesis. Emigrants had no lower individual rank position and did not come from lower-ranking matrilines. Emigrants had more female maternal relatives, especially sisters. Males without female relatives almost never emigrated. Conversely, there is virtually no indication that emigrants were evicted from the natal group. Emigrants had no increased mortality. Paternity data revealed that the reproductive success of emigrants and natal males is similar, indicating that emigration had no reproductive cost. Many similarities between emigrants and natal males that separated from female maternal kin during group fissions suggest that inner migration during fissions is an alternative way to avoid maternal inbreeding. The mating system resulted in a genetic structure within social groups that largely diminished the chances for paternal inbreeding even without recognizing paternal kin.     

Dispersal among male ring-tailed lemurs (Lemur catta) on St. Catherines Island

Male dispersal patterns were analyzed across a nine-year period in a population of ring-tailed lemurs (Lemur catta) on St. Catherines Island (SCI), USA, to evaluate two ultimate explanations for male dispersal: inbreeding avoidance and intrasexual mating competition. As part of this analysis, we also compared patterns of dispersal at this site with data from wild populations. Overall, we found that patterns of male intertroop movement on SCI are similar to the wild with respect to the frequency and seasonality of male transfer. In Madagascar, males move between groups every 3.1-3.5 years [Sussman, International Journal of Primatol 13:395-413, 1992; Koyama et al., Primates 43:291-314, 2002] as compared with every 3.2 years on SCI. The majority of transfers on SCI occurred during the birth season, as occurs at one site in Madagascar, Berenty [Budnitz & Dainis, Lemur biology. New York: Plenum Press, p 219-235, 1975; Jones, Folia Primatologica 40:145-160, 1983]. One difference is that males perform natal transfers 1-2 years earlier on SCI than in the wild, which may be related to food provisioning on SCI. Males never transferred back into their natal troops, which is remarkable given the small number of groups on SCI. Although this pattern of movement can indicate inbreeding avoidance by males, the fact that male troop tenure was in many cases long enough to overlap with the sexual maturation of potential daughters did not support the inbreeding avoidance hypothesis for male secondary dispersal. Instead, the intrasexual competition hypothesis was strongly supported, because males were significantly more likely to transfer into groups having fewer adult males and a more favorable sex ratio than their pretransfer groups. Males therefore appear to be bypassing groups in which they would experience a greater degree of intrasexual mating competition during the breeding season.     

Dispersal in sub-Saharan baboons.

In most mammalian species, males tend to leave their natal group and disperse farther than females, while females tend to be philopatric. Primates generally follow this rule, although long-term studies of a variety of species are revealing an increasing number of exceptions. This paper reviews dispersal patterns in 3 subspecies of savanna baboons (Papio cynocephalus cynocephalus, P. cynocephalus anubis, P. cynocephalus ursinus) which exhibit very similar patterns of social organization. Males usually disperse from the natal group at 8-10 years of age. Female dispersal is rare but well documented. Inbreeding avoidance as well as enhanced mating opportunities are suggested as ultimate causes of dispersal. Several proximate factors implicated in the timing of dispersal events are also reviewed.     

Patterns and dynamics of sex-biased dispersal in a nocturnal primate, the grey mouse lemur, Microcebus murinus

We examined predictions on the proportion of dispersing natal males and females, dispersal distances, the age at dispersal and the potential for inbreeding over a 6-year period in a free-living population of grey mouse lemurs. We used monthly mark-recapture procedures to determine individual locations and interindividual distances. The analysis of seven polymorphic microsatellite markers for 213 (130 males, 83 females) individuals allowed us to estimate relatedness coefficients and kinship relationships. Closely related males ranged further from each other than closely related females and natal males were found further from their potential mothers than were females. Natal males were more likely to disperse from their birth sites than females, although male dispersal was not universal. Male breeding dispersal was detected in half of the long-term observations. Males therefore seem to be the predominant vectors for gene flow between populations and social units. Females usually stayed within one to two home range diameters of their potential mother, facilitating the evolution of cooperative behaviour by kin selection among females. Most dispersal took place before the mating season, indicating an age of less than 7 months for natal dispersal. The analysis of spatiotemporal coexistence revealed the potential for inbreeding in only 3.8% of the potential mother-son dyads, but in 21.9% of the potential father-daughter dyads and in 41.7% of other closely related male-female dyads. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Natal Dispersal and Philopatry in the Carnivorous Marsupial Phascogale tapoatafa (Dasyuridae)

The proximate and ultimate causes of dispersal in semelparous carnivorous marsupials (Phascogalinae) have previously been hypothesized to be maternal aggression and inbreeding avoidance, respectively. This study tests these hypotheses by exposing 26 litters of Phascogale tapoatafa to a diverse range of social and environmental conditions that potentially affect dispersal (e.g. supplemental feeding, post-weaning desertion by the mother, orphaning, and release of subadults into unoccupied habitat). The mean dispersal age was 162 ± 5.6 d, which is about 3 wk after weaning is complete. Juvenile dispersal was strongly male biased under all conditions, suggesting that extrinsic proximate causes do not adequately account for male emigration. Home range establishment by males was contingent on the presence of females. Half of the monitored daughters were philopatric, and others typically settled adjacent to the natal site, thus possibly enhancing their reproductive potential by occupying an area of known resource quality. Because philopatry increases the risk of incest, females may be selected to preferentially mate with unrelated males (immigrants), when they are available, to avoid inbreeding. If so, the presence of immigrant males would reduce the probability of locally born, related males reproducing at their natal site. Thus inbreeding avoidance by females may create local mate competition among males and select for male dispersal. Emigration also ensured that males avoided inbreeding, but, if they dispersed into unoccupied habitat, male P. tapoatafa often returned to the natal area. This 'boomerang strategy' of returning to mate with related females suggests that, in the absence of conspecifics along the dispersal path of a male, mate competition will be weak at the natal site and female mate choice will not preclude related males. Thus while inbreeding avoidance by either or both sexes is perhaps the most parsimonious explanation of male-biased emigration, dispersal patterns were apparently strongly influenced by additional factors, so that the ultimate causation of the dispersal regime may be more complex.     

Why Be Vigilant? The Case of the Alpha Animal

We compared patterns of vigilance behavior in a male- and a female-dominant species—white-faced capuchins and ring-tailed lemurs—and used the results to test four hypotheses to explain vigilance behavior in primates. Adult male white-faced capuchins spent significantly more time vigilant than females did, and much male vigilance appeared to be directed toward males from other social groups. This finding supports the protection of paternity hypothesis. No sex difference existed in vigilance behavior among the ring-tailed lemurs, and subjects of both sexes exhibited more vigilance toward predators/potential predators than toward extragroup conspecifics, which supports the predator detection hypothesis. A trade-off argument, suggesting that females tolerate males in a group in return for greater male vigilance, does not apply to ring-tailed lemurs in our study. In both the male-dominant capuchins and the female-dominant ring-tailed lemurs, the alpha subject in the majority of the study groups was significantly more vigilant than other group members were. In white-faced capuchins, the alpha male mates more often than subordinate males do; therefore, the greater degree of vigilance exhibited by the alpha male may correspond to the protection of his reproductive investment. In ring-tailed lemurs, there can be more than one matriline in a group. Thus, the greater amount of vigilance behavior exhibited by the alpha female may be related to protection of her matriline, which could ultimately lead to greater inclusive fitness. Alpha subjects in our study groups exhibited certain behaviors more frequently or exclusively. Accordingly, there may be a constellation of behaviors characteristic of alpha animals.     

Male life history and intergroup mobility among ringtailed lemurs (Lemur catta)

Lemur catta shares a male-biased dispersal pattern with most primate species and the majority of mammals. Individuals in a free-ranging population of ringtailed lemurs were captured, marked, released, and monitored for a 40-month period. Sixty-four percent of the males (43 of 67) migrated or were missing within this period and all nine censused groups were affected by migration. Males migrate from their natal group and then may migrate again after reaching full adult body weight. Full-sized adult males migrate at a rate of 0.28 per year or once every 3.5 years and may change groups a number of times during their life. Migrations occurred within a 6-month period, ending just after the mating season. However, there is no direct connection between mating success and male migration. Females mate with transferring males, with group males, and with visitors from adjacent groups. The age-related pattern of male migration and the occurrence of extragroup mating inLemur catta is similar to that described for several species of macaques.     

Male intergroup mobility in a wild population of the Barbary macaque (Macaca sylvanus), Ghomaran rif mountains,Morocco

In this two-year study of a Barbary macaque population (n = 162) in the Ghomaran region of Morocco, 13 cases of males separated from their assumed natal groups were observed (nine visits of nonresident males to groups, two males isolated from groups as much as one day and one night, and two sets of snow tracks indicating males travel +7 km as isolates). Males left their assumed natal groups primarily in the mating season (12 cases), focused their interactions on estrous females of other groups, and were observed to copulate with these females in two cases. All males leaving their assumed natal groups were estimated to be between 5 and 8 years of age, with one exception (+ 15 years). It could not be determined whether males younger than 5 years moved between groups, or whether any males made permanent intergroup transfers. Regardless, the data from this study indicate that male intergroup mobility (and intergroup gene flow) was higher than has been previously assumed for this species. A prior theory that Barbary macaque groups are highly inbred, and that this is causally related to the evolution of male-infant care in this species, is not supported by the data of this study.     

Natal emigration by both sexes in the La Pacifica population of mantled howlers: when do some stay?

We have reported previously that all male and female mantled howlers emigrate from natal groups at Hacienda La Pacifica, Costa Rica. In the years since that report, a small number of juveniles have stayed in the natal group without experiencing a solitary phase. Here, we present a post hoc analysis on juvenile emigration in six groups of howlers under observation for varying amounts of time between 1972 and 2005. Our records revealed 139 juveniles for whom emigration status was certain, and 125 of these did emigrate. There was a significant association between presence of mother and emigration: juveniles without mothers were more likely to remain in their natal group (chi(1)(2) = 53.1, P<.0001). The mean age of emigration for all juveniles (n = 125) was 2.47 years (SD = 0.9, range = 1.5-6.5). There was no difference in age of emigration by adult male composition (one-male, multi-male, both), but juveniles of unknown sex emigrated younger than either known males or females (F(2,116) = 4.4, P<.02). For emigrating juveniles of known sex (n = 99), both males and females without mothers left at a later age than those with mothers (F(1,95) = 6.5, P<.02). Although philopatry or delayed emigration occurs in a few motherless animals, most males and females do emigrate from their natal groups at ages consistent with those reported for other species of howlers.     

Sex-biased dispersal in eastern chipmunks, Tamias striatus

I investigated the effect of male mate competition and inbreeding avoidance on natal dispersal of chipmunks by longitudinally monitoring known individuals from 1986 to 1990. Natal males exhibited greater absolute and effective dispersal distances but dispersed at the same proportion as natal females. Recruitment of juvenile males was negatively affected by density of resident males, but there was no evidence of local mate competition among male kin. Analysis of the spatial distribution of neighbors showed that natal males settled farther from their mothers than did their female siblings and farther than unrelated juvenile males. In addition, mothers apparently tolerated daughters as close neighbors and occasionally shared den sites with grandprogeny. Sexually mature males were never neighbors of their mothers and were never observed at maternal mating bouts. Males may disperse to improve reproductive opportunities by avoiding competition with resident males, and by increasing access to unrelated females. Maternal tolerance of daughters but not sons may result in the close affiliation between mothers and daughters, and indirectly contribute to dispersal of natal males. Hence male-biased dispersal could be a consequence of mate competition and maternal avoidance of incestuous matings. This revised version was published online in July 2006 with corrections to the Cover Date.     

Parental rank and reproductive success of natal rhesus males

In primates, the relationship between the ranks of parents and those of their sons has not been studied systematically, yet it has important implications for sociobiological theories. The influence of parents' ranks upon the ranks and reproductive success of their sons who remain and breed within their natal group was tested in two captive groups of rhesus macaques, Macaca mulatta. Paternity exclusion analyses revealed that both the rank and reproductive success of natal males were strongly associated with their mothers', but not their fathers', ranks. The ranks of natal males were also significantly correlated with their own reproductive success. However, this correlation was not nearly as strong as the correlation between the ranks and reproductive success of the fathers of these natal males. This difference was associated with a decline in reproductive success, but not in rank, of some founding males after natal males reached sexual maturity, and might result from an age bias in mating and/or the increase in the ratio of adult males to females. Although the reproductive advantage enjoyed by sons of high-ranking mothers prior to dispersal from their natal groups might be of evolutionary significance, it is important to determine whether or not this advantage persists after dispersal.     

Group changing in free-ranging male rhesus monkeys

Group changing behavior of maleMacaca mulatta was studied over a six-year period at the rhesus monkey colony on two coastal islands at La Parguera, Puerto Rico. Males first left their natal group at a mean age of 47 months and became solitary for the first time at a mean age of 64 months; all had left their natal groups by seven years of age. Age, mating season, sex ratios of adult males and females in the social bands, and geographical barriers all had significant effects on the group shifting. Population size, rank of mother or being an orphan did not significantly affect the changing process. Two factors, age (size) and seniority in the group, were important in determining a male's rank in his new group.     

Mating system and sex allocation in the gregarious parasitoid Cotesia glomerata

The gregarious parasitoid Cotesia glomerata (L.) is often presumed to possess the characteristic attributes of a species that manifests local mate competition (LMC), as it commonly produces female-biased broods. However, our field surveys of sex ratio and laboratory observations of adult behaviour showed that this species is subject to partial local mate competition caused by natal dispersal. On average, 30% of males left their natal patch before mating, with the proportion of dispersing males increasing with an increase in the patch's sex ratio (i.e. proportion of males). Over 50% of females left their natal patch before mating, and only 27.5% of females mated with males emerging from the same natal patch. Although females showed no preference between males that were and were not their siblings, broods from females that mated with siblings had a significantly higher mean brood sex ratio (0.56) than broods from females that mated with nonsiblings (0.39). Furthermore, brood sex ratios increased as inbreeding was intensified over four generations. A field population of this wasp had a mean brood sex ratio of 0.35 over 3 years, which conformed well to the evolutionarily stable strategy sex ratio (r=0.34) predicted by Taylor's partial sibmating model for haplodiploid species. These results suggest that the sex allocation strategy of C. glomerata is based on both partial local mate competition in males and inbreeding avoidance in females. In turn, this mating system plays a role in the evolution of natal dispersal behaviour in this species.Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Male Behavior and Regulation of Worker Mating in a Ponerine Ant, Pachycondyla (Bothroponera) sp. (Hymenoptera: Formicidae)

Male behavior and regulation of worker mating were observed in Indonesian Pachycondyla sp. The colonies had some mated workers but only one gamergate (mated and egg-laying workers). Males frequently tried to mate with workers in their natal nests irrespective of worker age and dominance rank, however, workers never accepted mounting of nestmate males. Worker mating occurred only under the gamergateless condition with alien males.     

Life history and demography of wild moor macaques (Macaca maurus): summary of ten years of observations

Data on the life history and demography of individual species are indispensable when we discuss social behavior from an evolutionary perspective, and when we attempt to make adequate conservation plans. This is the first report on the life history and demography of moor macaques in their natural habitat. Moor macaques (Macaca maurus) in the Karaenta Nature Reserve, South Sulawesi, Indonesia, have been observed since 1981. Individual identification of group members began in 1988. The size of the study group increased continuously, from 20 to 43, over this 10-year period of observation (1988-1998). The average population growth rate was 8.0%, and 45 births were confirmed during this period. They were categorized as moderately seasonal breeders. Mortality rate within one year after birth was 17.1%. Average inter-birth interval following surviving infants was 24.1 months, while that following early infant death was 15.0 months. As is the case in other species of macaques, males moved between groups while females stayed in their natal groups. Females seemed to exhibit their first perineal swelling at 4-6 years of age, and to have their first infant at 6-7 years. Males left their natal group at 7-9 years. Solitary males were seldom observed around the study group. The late dispersal of males from their natal groups and their infrequent movement between groups contrast with patterns in well-known macaque species such as Japanese macaques. Recently, differences in social characteristics among macaque species have attracted the attention of researchers. Our findings would be useful to further understanding of such social differences.     

Mating patterns, relatedness and the basis of natal philopatry in the brown long-eared bat, Plecotus auritus

The brown long-eared bat, Plecotus auritus, is unusual among temperate zone bats in that summer maternity colonies are composed of adult males and females, with both sexes displaying natal philopatry and long-term association with a colony. Here, we describe the use of microsatellite analysis to investigate colony relatedness and mating patterns, with the aim of identifying the evolutionary determinants of social organization in P. auritus. Mean colony relatedness was found to be low (R=0.033 +/- 0.002), with pairwise estimates of R within colonies ranging from -0.4 to 0.9. The proportion of young fathered by males in their own colony was investigated using a Bayesian approach, incorporating parameters detailing the number of untyped individuals. This analysis revealed that most offspring were fathered by males originating from a different colony to their own. In addition, we determined that the number of paternal half-sibs among cohorts of young was low, inferring little or no skew in male reproductive success. The results of this study suggest that kin selection cannot account for colony stability and natal philopatry in P. auritus, which may instead be explained by advantages accrued through the use of familiar and successful roost sites, and through long-term associations with conspecifics. Moreover, because the underlying causes of male natal dispersal in mammals, such as risk of inbreeding or competition for mates, appear to be avoided via extra-colony copulation and low male reproductive skew, both P. auritus males and females are able to benefit from long-term association with the natal colony.     

Movement patterns of the White-tailed Sea Eagle (Haliaeetus albicilla): post-fledging behaviour,natal dispersal onset and the role of the natal environment

Exploratory movements and natal dispersal form essential processes during early life history stages of raptors, but identifying the factors shaping individual movement decisions is challenging. Global positioning system (GPS) telemetry thereby provides a promising technique to study movement patterns on adequate spatio-temporal scales. We analysed data of juvenile White-tailed Sea Eagles Haliaeetus albicilla (WTSE) in north-east Germany (n = 24) derived from GPS tracking to extensively analyse movements between fledging and emigration from the natal territory. Our goal was to determine the time point of fledging, characterize pre-emigration movements and the onset of natal dispersal while investigating the influence of the natal environment. WTSE fledged at an average age of 72 days and showed strong excursive behaviour during the post-fledging period regarding the number, distance and duration of excursions, yet with high individual variability. Excursive behaviour did not differ between sexes. On average, WTSE left the parental territory 93 days after fledging. The quantity of excursive behaviour delayed the timing of emigration and WTSE tended to postpone their emigration when foraging water was accessible within the boundaries of their parental territory. The overall results suggest that young WTSE assess the quality of the natal environment via pre-emigration movements and stay in their territory of origin for as long as internal and external conditions allow for it. Our study is one of the first to characterize post-fledging and natal dispersal movements of young WTSE to such an extent and applies modern techniques to understand related movements in relation to the natal environment. The results emphasize the urgent necessity for the extension of currently existing nest protection periods and guaranteeing sustainable management of potential breeding and foraging grounds for WTSE. Ultimately, the results are relevant for all large raptor species sensitive to human-related disturbance, as they support the increasing importance of regulations with spatio-temporal specifications for breeding populations of large raptors in densely human-inhabited areas with increasing alteration of land.