Male philopatry in spider monkeys revisited

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 00:00–00 (2013) Male Philopatry in Spider Monkeys Revisited Filippo Aureli,1,2* Anthony Di Fiore,3 Evin Murillo-Chacon,4 Shoji Kawamura,5 and Colleen M. Schaffner1,6 1 Instituto de Neuroetologıa, Universidad Veracruzana, Xalapa 91190, Mexico Research Centre in Evolutionary Anthropology and Palaeoecology, Liverpool John Moores University, L3 3AF, Liverpool, UK 3 Department of Anthropology, University of Texas at Austin, Austin, TX 78712 4  Santa Rosa Sector, Area de Conservacion Guanacaste, Liberia 169-5000, Costa Rica 5 Department of Integrated Biosciences, University of Tokyo, Kashiwa, 277-8562, Japan 6 Department of Psychology, University of Chester, Chester CH1 4BJ, UK 2 KEY WORDS system Ateles geoffroyi; dispersal; immigration; male–male relationships; social ABSTRACT Dispersal patterns are critical for understanding social systems as they influence social interactions and relationships. Spider monkeys (Ateles spp.) are typically described as being characterized by male philopatry and female dispersal, with these patterns reflected in stronger affiliative and cooperative relationships among males than among females. Recent findings, however, indicate that male–male relationships may not be as uniformly strong as previously thought, which suggests that male philopatry in spider monkeys may not be universal. Here, we report the first confirmed cases of male immigration and group takeover in spider monkeys. Data were collected on one community of Ateles geoffroyi in northwestern Costa Rica. Behavioral and demographic data were recorded during subgroup follows across 6.5 years, and fecal samples of community members were collected for genetic analysis of related- Data on nonhuman primates accumulated up to the mid-1980s led to the view that in the majority of species males leave their natal group at puberty, whereas females remain philopatric, growing up and reproducing in their natal groups where they are often surrounded by same-sex kin (Moore, 1984; Pusey and Parker, 1987). This “typical primate” pattern was largely based on the knowledge of a few species of cercopithecines, the most studied taxa at that time (Melnick and Pearl, 1987; Strier, 1994a). However, as long-term field studies of other taxa proliferated, researchers came to the realization that social systems characterized by female philopatry and male dispersal are, in fact, mostly restricted to baboons, macaques, and a few other cercopithecine monkeys (Moore, 1984; Di Fiore and Rendall, 1994) and, therefore, that such a “typical primate” social system was a myth (Strier, 1994a). Among group-living mammals like primates, dispersal patterns are expected to affect within-group social interactions, especially the role that kinship can play in such interactions (Wrangham, 1980; Gouzoules and Gouzoules, 1987; Pusey and Parker, 1987; Moore, 1992; Di Fiore and Rendall, 1994; Isbell, 2004; Strier, 2008; Di Fiore, 2009). For example, philopatric macaque and baboon females tend to maintain strong, long-lasting relationships with other female kin, which form the core of their matrilineally structured groups and provide fitness benefits (Thierry, 2007; Silk et al., 2009, 2010), Ó 2013 WILEY PERIODICALS, INC. ness. We documented two separate cases of immigration involving multiple males, which resulted in take-over of the study community by extra-community males and the concomitant disappearance of the resident males. In the study community, males were no more closely related to one another, on average, than females were, contrary to what would be expected if males were the more philopatric sex. Comparison of corrected assignment indices for males and females also revealed no evidence of sexbiased dispersal. Our findings suggest that in spider monkeys male immigration may occur under certain demographic circumstances, contributing to a view of greater flexibility in their social system than previously appreciated. This discovery has implications for other species that are typically characterized by male philopatry. Am J Phys Anthropol 000:000–000, 2013. VC 2013 Wiley Periodicals, Inc. whereas relationships between dispersing males are largely indifferent or antagonistic. Conversely, stronger relationships among males are seen more commonly in species where males are philopatric (van Hooff, 2000; van Schaik and Aureli, 2000; Di Fiore et al., 2009; Mitani, 2009). Thus, dispersal patterns are critical for understanding social systems. Spider monkeys (Ateles spp.) live in a social system characterized by a high degree of fission–fusion dynamics in which community members are rarely all together, but split and merge into fluid subgroups with variable Grant sponsor: National Geographic Society; Grant number: 8825-10 and 9288-13; Grant sponsor: North of England Zoological Society; Grant sponsor: British Academy; Grant number: SG 32794, LRG 35389; Grant sponsor: Leakey Foundation. *Correspondence to: Filippo Aureli, Instituto de Neuroetologıa, Universidad Veracruzana, Av. Dr. Castelazo Ayala S/N, Col. Industrial Animas. Ap 566, Cp 91190, Xalapa, Veracruz, M exico. E-mail: [email protected] or [email protected] Received 1 February 2013; accepted 10 June 2013 DOI: 10.1002/ajpa.22331 Published online 00 Month 2013 in Wiley Online Library (wileyonlinelibrary.com). 2 F. AURELI ET AL. membership (Symington, 1990; Chapman et al., 1995; cf. Aureli et al., 2008; Di Fiore et al., 2011). Among primates, this social system is also characteristic of hominoid taxa, such as chimpanzees (Pan troglodytes), bonobos (Pan paniscus; Nishida and Hiraiwa-Hasegawa, 1987; Stumpf, 2011), and humans (Rodseth et al., 1991; Marlowe, 2005). As spider monkeys are New World primates, they offer an opportunity to study convergent evolution and may provide insight into the principles of hominoid social evolution. Like chimpanzees and bonobos, spider monkeys are typically described as being characterized by male philopatry and female dispersal (Symington, 1988; Strier, 1994b; Shimooka et al., 2008; Di Fiore et al., 2011). In fact, a recent review of dispersal patterns among spider monkeys pointed out that all reported cases of immigration involved females, and that most females left their natal community before reproducing (Shimooka et al., 2008). In addition, genetic analysis of a large group of white-bellied spider monkeys (A. belzebuth) living in an undisturbed habitat found that adult males were, on average, more related to each other than were adult females, confirming that the core of Ateles communities consists of related, philopatric males, whereas females disperse into other communities as they approach sexual maturity (Di Fiore et al., 2009). These sex-biased dispersal patterns are mirrored by findings of stronger affiliative and cooperative relationships between males than between females (Fedigan and Baxter, 1984; Symington, 1990; Ahumada, 1992; Slater et al., 2009; Di Fiore et al., 2011). Recent field observations, however, suggest that male–male relationships may not be as consistently and uniformly strong as previously thought (Aureli and Schaffner, 2008). For example, in A. geoffroyi some male–male social relationships are tenuous and prone to risk, as evidenced by relatively high rates of exchanges between males of behaviors associated with appeasement and aggression (Rebecchini et al., 2011; Schaffner et al., 2012). Here, we report the first confirmed instances of male immigration in spider monkeys. We first describe two separate cases involving multiple males, which resulted in the take-over of the study community by extracommunity males and the concomitant disappearance of the resident adult males. We then use genetic data to examine the degree of relatedness among males and among females in the study community, as well as among cohorts of immigrating males, in order to better understand the level of male philopatry. The immigration patterns, their consequences, and other events involving extra-community males depict a picture of risky relationships and ephemeral alliances among males, and suggest greater flexibility in the social system of spider monkeys than heretofore appreciated. METHODS Study site and community The study was carried out in the Santa Rosa Sector of  the Area de Conservacion Guanacaste, northwestern Costa Rica. The site comprises 108 km2 of tropical dry forest covering an upper and lower plateau and ranging from the foothills of volcanic mountains down to the Pacific coastal plain (0–300 m elevation). Rainfall is highly seasonal, with a severe dry period between December and May and a wet season during the rest of American Journal of Physical Anthropology the year when most of the annual rainfall occurs (900– 2500 mm) (Janzen, 1986). Since 2000, we have studied one community of spider monkeys (Ateles geoffroyi), all of whom are well habituated to being followed by researchers and are individually recognized using size, pelage, and facial patterns. During the study period, community size varied between 25 and 34 individuals (2–8 adult and subadult males, 15–18 adult and subadult females, 3 to 7 juveniles, and 2 to 9 infants) due to births, immigrations, and disappearances. Following other research on spider monkeys, a male was considered a subadult when it was typically older than 5 years and sexually mature (i.e., his testicles were no longer close to the body as is the case in younger males) but had not yet achieved full adult size (van Roosmalen and Klein, 1988; Campbell and Gibson, 2008; Shimooka et al., 2008). Observational methods The observations reported here spanned more than 6.5 years, from April 2003 until December 2009. Over this period, we conducted follows of spider monkey subgroups three to five days per week during the entire course of daylight hours, attempting to balance observations between mornings and afternoons. Individual spider monkeys were considered to be in the same subgroup when they were seen at a distance of  50 m from at least one other subgroup member (Asensio et al., 2009; Aureli et al., 2012). “Fissions” occurred when one or more individuals from a followed subgroup were not observed at a distance of  50 m from at least one current subgroup member for more than 30 minutes. “Fusions” occurred when one or more individuals not belonging to a followed subgroup approached to within a distance of  50 m from any member of a followed subgroup. After a fission event, we randomly selected which subgroup to continue following. The location of the followed subgroup was automatically recorded every minute using the track point setting on a handheld global positioning unit (Garmin GPSMAP 76CSX) from roughly the center of the subgroup. These location records were subsequently used to determine the community’s home range (Asensio et al., 2012). A combination of sampling methods (Altmann, 1974) was used to collect behavioral data on activity and social interactions: 10-minutes instantaneous sampling of all visible subgroup members in which their activities and proximity (within an arm reach) with other individuals were scored; all-occurrence sampling of conspicuous events, such as fissions, fusions, and escalated aggression; and ad libitum sampling of approaches, grooming, play, and three additional typical spider monkey behaviors, “embraces,” “arm-wrapping,” and “grappling” (van Roosmalen and Klein, 1988; Slater et al., 2009; Schaffner et al., 2012). “Embraces” (i.e., where an individual places its arm around the neck or back of another individual while facing the recipient, typically lasting only a few seconds) are most commonly observed at times when animals are at greater risk of aggression from conspecifics, such as during fusion events (when aggression is more likely: Aureli and Schaffner, 2007) or when mothers with vulnerable infants are approached by other adults (Schaffner and Aureli, 2005; Slater et al., 2007). This behavior seems to indicate a willingness for positive interaction and thus to reduce risk during these instances. “Arm-wrapping” (i.e., where each individual places 3 MALE IMMIGRATION IN SPIDER MONKEYS an arm around the partner’s back while both are facing forward and jointly threatening a third party) is a coalitionary behavior manifest during aggressive situations. “Grappling” (i.e., where animals engage in a prolonged exchange of physical contact that can involve facial greeting, face touching, tail wrapping, pectoral sniffing, genital contact, and embraces) appears to occur typically between males when there is strong attraction on the part of a younger male toward an older male, in conjunction with a substantial risk to the younger male (Aureli and Schaffner, 2008; Vick, 2008; Schaffner et al., 2012) due to aggression it can receive from older males, which can even have lethal consequences (Campbell, 2006; Valero et al., 2006; Vick, 2008). All of these types of data were recorded into a dictaphone and then transcribed into a computer database within 1–3 days of being collected. The use of dictaphones also allowed observers to record a detailed account of any additional events, such as encounters with extra-community monkeys. Relatedness analysis Replicate fecal samples of all community members were obtained as individually recognized animals defecated during observations. Samples were placed in 15-ml plastic vials preloaded with either 5 ml of ASL lysis buffer (QIAamp DNA Stool Mini Kit; Qiagen, Crawley, UK) or RNALaterTM (Ambion) nucleic acid preservation buffer. Immediately following collection, the feces-buffer mixture was homogenized by shaking and then stored at room temperature until being shipped to Japan for extraction. DNA was extracted from samples of all individuals of reproductive age (10 males and 20 females) using the QIAamp DNA Stool Mini Kit (see Hiramatsu et al., 2005 for details). DNA samples were then genotyped at a panel of 11 polymorphic SSR loci (Table 1) (Di Fiore et al., 2009). On the basis of observed allele frequencies in the sampled monkeys across the set of typed loci, the complete panel yields a probability of identity between full siblings (PIID(sib)) value of 1.2 3 1024. The panel PIID(sib) value is calculated as the product across all loci of X X X 0:251ð0:5 p2i Þ1½0:5 ð p2i Þ2 Š2ð0:25 p4i Þ TABLE 1. Panel of markers used for genotyping D17S804 D8S165 D8S260 Leon 2 Leon 21 LL 1-1#10 LL 1-1#18 LL 1-5#7 Locus 5 SB 30 SB 38 Average N Na Allele size range Ho He Significance 30 30 30 30 30 30 30 30 30 30 30 0.167 0.700 0.767 0.900 0.867 0.733 0.600 0.867 0.600 0.567 0.833 0.691 0.156 0.721 0.813 0.796 0.842 0.709 0.612 0.772 0.529 0.567 0.853 0.670 NS NS NS NS NS NS NS NS NS NS NS 3 6 8 7 8 6 8 9 7 6 9 7 144–148 130–142 216–240 189–207 365–387 215–226 132–157 222–243 104–138 82–107 136–153 Allele size range values are in base pairs (bp). N, number of individuals genotyped. Na, number of alleles. Ho, observed heterozyogosity. He, expected heterozyogosity under Hardy–Weinberg equilibrium. NS, no significant difference between observed and expected genotype frequencies. th where pi 5 the frequency of the i allele at each locus (Evett and Weir, 1998; Taberlet and Luikart, 1999; Waits et al. 2001). The low value for PIID(sib) highlights the very low probability that any two individuals, even full siblings, would be expected to share the same multilocus genotype by chance. Loci were genotyped in either single-plex or multiplex PCR reactions using commercially available kits (Qiagen Multiplex PCR Kit) following previously published reaction conditions and cycling profiles (see Di Fiore et al., 2009 for details). PCR products were mixed with a fluorescently labeled size standard (GeneScan 500 [ROX]) and then separated and visualized on an ABI 3730 automated DNA Analyzer. Allele sizes were initially called using the software GeneMapper 4.0 and then reviewed by eye to remove spurious peaks and confirm allele calls. Individual x locus genotypes were confirmed by replicating putative heterozygotes at least twice from two separate PCR reactions and by replicating putative homozygotes in least four separate reactions, using from two to four separate extractions per individual. Using these multilocus genotypes, an estimate of genetic relatedness was calculated for every pair of sampled individuals using Queller and Goodnight’s (1989) regression-based relatedness estimator as implemented in the software package GenAlEx 6 (Peakall and Smouse, 2006). This estimator ranges from 21 to 11, where positive values indicate pairs of individuals who are genetically more similar to one another than expected given background allele frequencies in a population, whereas negative values indicate animals that are genetically less similar than expected by chance. We used these estimates to calculate the average estimated relatedness among different sets of individuals, including all community adult females, all community adult males, and cohorts of immigrant males. Permutation tests were used to evaluate the significance of differences in mean relatedness values among males versus among females (Vigilant et al., 2001; Di Fiore and Fleischer, 2005). Finally, we used assignment indices (AI) to summarize the likelihood that an individual’s multilocus genotype originated in the population in which it was sampled (Paetkau et al., 1995). When assignment indices are standardized by subtracting the mean assignment index for the population from each individual’s AI (Favre et al., 1997), animals with positive “corrected” assignment index (AIc) values are those more likely to have been born in the population, whereas those with negative AIc values are more likely to be immigrants. As members of the dispersing sex should show significantly lower AIc scores than members of the more philopatric sex (Favre et al., 1997; Lawson Handley and Perrin, 2007), we calculated AIc scores of the 10 males and 20 females using GenAlEx 6 (Peakall and Smouse, 2006) and compared them with a Mann–Whitney test. RESULTS We witnessed two cases of male immigration, each involving multiple males (Fig. 1). The first case involved three males, who were observed for the first time on February 2nd, 2005. At that time, apart from small juveniles and infants, there were only two males present in the study community, an adult male and a roughly 4-year-old juvenile male. In the preceding years, the number of males in the community had decreased, with one adult male disappearing in April 2003 and a large American Journal of Physical Anthropology 4 F. AURELI ET AL. Fig. 1. Presence of (sub)adult males in the study community from January 2005 until December 2009. Each bar represents the period of time each male was present in the community. Original males refer to the males that were in the community from the beginning of the study; 2005-A, 2005-B, and 2005-C refer to the males that immigrated in the study community in early 2005; 2006-A, 2006-B, 2006-C, 2006-D, and 2006-E refer to the males that immigrated in the study community in early 2006. No natal male reached subadult status during the study period. Dotted lines at the ends of the bars signify that males either were already present in the community before the study started (Original Males) or remained in the community after the end of the study (2005-B, 2006-D, and 2006-E). subadult male seen for the last time on December 6th, 2004. The second immigration case involved five males, who were observed for the first time on January 5th, 2006. Below we describe in detail the two cases and other relevant observations. Case 1 On February 2nd, 2005, we witnessed a fusion between the subgroup being followed, which consisted of adult females and their offspring, and another subgroup, which included the resident adult and juvenile males, several adult females and their offspring and three unknown subadult males who had never been seen before. These three males were clearly afraid of the researchers and shook branches and threatened them. One of the three subadult males arm-wrapped with the resident adult and juvenile males while threatening the researchers. The juvenile male was observed playing with one of the three subadult males before the resident adult male and the three unfamiliar subadult males fissioned from the remaining individuals. About 3 hours later, the resident adult male and the three subadult males rejoined the larger subgroup containing several females and their offspring. At that time, we did not witness any hostility between the three unfamiliar subadult males and members of the study community. Thus, this was probably not the first time the three unknown subadult males associated with members of the study community. Over the next few days, the three unfamiliar subadult males were often seen with members of the study community. They were again seen ranging with the resident adult male in the absence of other community members, and they were also seen in subgroups containing other community members, but without the resident male. On February 15th, when following a subgroup consisting of the resident adult and juvenile males and two of the American Journal of Physical Anthropology three subadult males, we observed embraces between the subadult males and the resident adult male. Beginning in April 2005, we started to see the resident adult and juvenile males traveling in a subgroup by themselves, although they were also found in subgroups with the community females both with and without the three subadult males. We also noted that the resident adult male started to show uneasiness about being with the three subadult males, monitoring them, moving away from them as they drew near, and vocalizing. On May 8th, the three subadult males arm-wrapped while threatening and pursuing the resident adult male, who moved away and kept himself at distance from them. On May 15th, we found the resident juvenile male injured and traveling alone. On May 26th, we followed a subgroup comprising only the resident adult and juvenile males for about 3 hours, and when one of the three subadult males joined the subgroup, the juvenile male fissioned away from the others. The two remaining males showed signs of tension and vocalized until the immigrant subadult male approached and embraced the resident adult male. At this point, the vocalizations ended, but the two males separated and kept at a distance from one another. About an hour later, the juvenile male, his putative mother, and two other adult females with offspring joined the two males, and 20 minutes later the juvenile male embraced the immigrant subadult male. In the following months, the association patterns of the males continued to be variable, with the two resident males being seen sometimes in subgroups with the community females, both with and without the three immigrant subadult males, but also seen traveling by themselves. August 23rd was the last day we saw the two resident males traveling with any of the community females. After having slept apart from the rest of the community members on August 30th, they started to move the next morning very early and fast. We have never seen them again. The three immigrant subadult MALE IMMIGRATION IN SPIDER MONKEYS males continued to associate with the females and to use the entire home range of the study community. We labeled these individuals the “2005 males” (2005-A, 2005-B and 2005-C). Case 2 On January 5th, 2006 we encountered a subgroup consisting of four females, their offspring, and five unfamiliar males whom we had never seen before. Four of these males were adults; the remaining male was a subadult. We labeled these individuals the “2006 males” (2006-A through 2006-E). These males were clearly afraid of the researchers and shook branches and threatened us, also forming coalitions by arm-wrapping with one another. The community adult females showed signs of apprehension by vocalizing and keeping at a distance from the 2006 males. On January 16th, four of the 2006 males were found early in the morning with many of the community adult females at one of the sleeping areas within the community home range. Also present was an unfamiliar adult female (with an infant) who did not show signs of apprehension toward the 2006 males. During the early morning, these monkeys all traveled together, and at one point the 2006 males jointly harassed a community adult female and her 2-year-old juvenile male. The 2006 males, the unfamiliar female, and some community females with their offspring fissioned from the followed subgroup consisting of community females and their offspring for about 1.5 hours. When the two subgroups rejoined one another, the adult females of the subgroup we were following vocalized and moved away from the 2006 males. About half an hour after the fusion, the 2year-old juvenile male and the 2006 subadult male grappled for 20 minutes. Forty-five minutes later the 2006 males and the unfamiliar female with the infant fissioned from the subgroup. For the next three months, the 2006 males were never seen, and the adult females from our study community associated regularly with the 2005 males. On April 20th, when four of the 2006 males joined a subgroup with several community adult females and their offspring, the females vocalized loudly. After 20 minutes, the 2006 males left the subgroup. On April 24th and 28th, the 2006 males were found with adult females from the community and their offspring at one of the community’s sleeping areas. One of the 2006 adult males exchanged an embrace with one of the community females, and the 2006 subadult male played with a juvenile female from the community. At this time, the 2006 males also chased some community females. On both days, the 2006 males and the community females traveled and fed all together for over an hour, until the 2006 males fissioned from the subgroup. In the following months, the 2006 males continued to associate with community females, who gradually became more and more tolerant of them, whereas the 2005 males were rarely seen. Male 2005-A was seen for the last time on June 13th, 2006, and male 2005-B started to range only on the northern side of the community’s territory. On September 4th, 2006, male 2005-C was found with community females. When three of the 2006 males joined with that subgroup near one of the community’s sleeping areas in late afternoon, 2005-C moved rapidly away, but then returned to sleep with the mix-sexed subgroup. This was the first time 2005 and 5 2006 males were seen in the same subgroup. On September 16th, we found 2005-C in a subgroup with two of the 2006 males and several community females. Male 2005-C did not avoid the two 2006 males, who fissioned from the subgroup after 3 hours, whereas male 2005-C stayed with the females. In the next few months, male 2005-C was rarely seen, but when he was he continued to easily associate with the females and the 2006 males. On April 12th, 2007, in the northern part of the community territory, we found male 2005-C within a mix-sexed subgroup including male 2005-B, but no 2006 males. From August 2007 on, males 2005-B and 2005-C have associated regularly with each other and have started to use the entire home range again, but without ever associating with any 2006 males. Subsequently, the community females were seen associating with either the remaining two 2005 males or the 2006 males, but never with members of both cohorts of males as the same time. Observations of other extra-community males Since 2003, we have had several encounters with other unfamiliar males within the home range of our main study community that suggest the possibility of male dispersal and transfer. In July 2003, we encountered two easily recognizable subadult males. Over the subsequent months, we never saw them associating with any community members; therefore, we did not consider them as belonging to the study community. We could recognize them individually and follow them easily on multiple occasions. They ranged in the southern part of the community home range and spent most of their time in the company of one another or with a group of whitefaced capuchin monkeys (Cebus capucinus). We saw them for the last time on May 23rd, 2004. On October 27th, 2003 we encountered an unfamiliar subadult male in a subgroup with multiple community females. The subadult male had fresh wounds on his shoulders and back, which several of the females licked. He traveled, fed and rested with the subgroup for several hours before fissioning off with some of the females. No adult or subadult male of the study community joined the subgroup during the time the wounded subadult male was there. We have never seen this male again. On March 29th, 2005 an unfamiliar subadult male and two subadult females from the study community joined a subgroup we were following that contained the resident adult and juvenile males, but as soon as the unfamiliar subadult saw the resident adult male, he descended to the ground and started to quickly move away. The resident adult and juvenile males fissioned from the females and followed the unfamiliar subadult male for 25 minutes. The unfamiliar subadult male walked on the ground the entire time, whereas the resident adult male moved on the ground only a few times tracking the unknown subadult. This is an unusual behavior given that spider monkeys are highly arboreal, but it is effective in reducing conspicuousness when moving (Campbell et al., 2005; Aureli et al., 2006). We have never seen this unknown male again. The epilogue By the middle of 2008, two of the five 2006 males were no longer regularly seen at the study site (Fig. 1). The remaining males occupying the community home range fell into two cohorts, with the males of each cohort American Journal of Physical Anthropology 6 F. AURELI ET AL. associating mostly together and never with members of the other cohort. One cohort consisted of the three remaining 2006 males (2006-C, 2006-D, and 2006-E), who often associated with the females. The other cohort was made up of the two remaining 2005 males (2005-B and 2005-C), who were not seen often, but on occasion associated with community females and used the entire community home range. In April 2009, male 2006-C disappeared, and in June 2009, male 2005-C disappeared, leaving only two 2006 males and male 2005-B. On September 10th, 2009 we found these three males in a subgroup together. This was the first time we recorded any of the 2005 and 2006 males in the same subgroup since the brief period at the end of 2006 described earlier in which 2005-C was seen associating with 2006 males. We observed a few coalitionary attacks by the two 2006 males and a 4.5-year-old juvenile male against 2005-B, but the latter kept himself at a safe distance and traveled with the mixed-sex subgroups for several hours. Similar observations were made during the following days when we followed these males together several times. On October 5th, the two 2006 males, 2005B and two juvenile males older than 4 years were seen together in an all-male subgroup, which is typical in spider monkeys when males travel to patrol territory boundaries (Aureli et al., 2006; Wallace, 2008). On October 7th, we observed for the first time an embrace between 2005-B and one of the 2006 males. The following day, these two males teamed up and threatened the researchers while arm-wrapping. During subsequent days, we observed a few mild aggressive exchanges between 2006 males and 2005-B, but also some embraces. In the following months the remaining three males from the 2005 and 2006 immigrations were regularly seen together. Relatedness The average estimated relatedness (mean R) among the 10 males of reproductive age who were in the study community between 2003 and 2009 (two original males, three 2005 males and five 2006 males) was 0.013 (SD: 6 0.195), whereas that among the equivalent 20 females was 20.039 (60.188). There was no significant difference between the mean R among males and that among females (permutation test: P 5 0.076). That is, as a group, males were no more closely related to one another, on average, than females were, contrary to what would be expected for the more philopatric sex. Similarly, comparison of corrected assignment indices for males and females sampled in the study community across this 6.5-year period revealed no evidence of sexbiased dispersal. AIc scores for both males and females averaged close to zero (Fig. 2), and there was no signifi- Fig. 2. Mean (6SD) corrected assignment index (AIc) values for community males and females. American Journal of Physical Anthropology cant difference in the mean AIc between males and females (N1 5 10, N2 5 20, z 5 0.484, P 5 0.628). Finally, the mean R among the three 2005 immigrant males (0.018 6 0.103) and that among the 2006 immigrant males (0.064 6 0.186) were also not significantly different from that among females (2005 males: P 5 0.375; 2006 males: P 5 0.059). That is, cohorts of immigrant males were not particularly closely related to one another relative to other animals in the community, although one 2006 male had relatively high estimated R with three males of the same cohort. DISCUSSION Over the course of 6.5 years, between 2003 and 2009, the male composition of the study community of spider monkeys changed radically. The three (sub) adult males that were present in 2003 all disappeared by September 2005, along with a juvenile male. This left the community without any resident natal males. These males were replaced by three males, who immigrated in February 2005 and who were joined by five additional immigrant males the following year. To the best of our knowledge, a similar series of events has never been reported for any other community of spider monkeys. Genetic data characterizing the entire set of males and females of reproductive age sampled across this time frame revealed a similar average degree of relatedness among males and among females and no difference in mean male versus female assignment indices, a pattern consistent with a lack of sex-bias in dispersal. Males of the same immigrating cohort had overall a low degree of relatedness with one another, but one 2006 male was closely related to three males of the same cohort. Although the two cohorts of new males associated with one another only rarely (only one 2005 male was observed to associate with 2006 males a few times), they did coexist in the home range of the study community and associated with the same set of females. Possibly due to the disappearance of members of each male cohort, by September 2009 one 2005 male and two 2006 males joined forces, becoming the resident males of the study community. Overall, the interactions between the original (and possibly natal) males and the 2005 immigrant males, and between the 2005 and the 2006 males, were only partially antagonistic, and males from different cohorts could, at times, associate in the same subgroup for long periods. Additionally, coalitions between immigrant males, even when not closely related, played an important role, but the supplanting and replacement of the original males by the 2005 immigrants was a prolonged process that lasted several months. Similarly, the integration of the 2005 and 2006 males into a final, successful cohort of three males lasted over three years. Thus, we witnessed slow and somewhat subtle processes, which differ markedly from male takeovers in species where male immigration is typical (LaBelle et al., 2008; Cords and Fuller, 2010; Zhao et al., 2011). For example, group takeover by immigrant males is a relatively frequent, rapid, and bloody affair in white-faced capuchin monkeys, which live sympatrically to the study spider monkeys (Fedigan and Jack, 2004; Jack et al., 2012). The report of rare events, such as male immigrations, within a well-known demographic and well-documented behavioral and genetic context is one of the benefits of long-term studies on identified individuals (Kappeler MALE IMMIGRATION IN SPIDER MONKEYS and Watts, 2012). The reason we were able to document the occurrence of male immigrations and takeover is probably due to the long-term nature of our project. Similar rare events may occur at other sites, but possible instances of male immigration might go unnoticed because they are difficult to identify and document during field projects that are not continuous or tend to last only a few years. Still, genetic data suggest possible cases of immigration in other spider monkeys. For example, in one large community of white-bellied spider monkeys, one of the resident adult males was unrelated to any of the remaining adult males and in a second community, the average estimated relatedness among male– male dyads was low, implying that in at least some cases male spider monkeys may disperse and join new communities (Di Fiore et al., 2009). In other species that are typically considered “malephilopatric,” there is also some evidence for rare male immigration. In lowland woolly monkeys (Lagothrix poeppigii), for example, molecular analyses and observations of solitary and bachelor males suggest that at least some males may disperse from their natal groups (Di Fiore and Fleischer, 2005; Di Fiore et al., 2009). In another atelin species, the northern muriqui (Brachyteles hypoxanthus), no case of male immigration has been observed during the 30-year project, but the existence of an all-male unit suggests possible male dispersal (Strier et al., 2006; Karen Strier, personal communication). Western red colobus (Procolobus badius badius) are also known for male philopatry (Struhsaker, 1975). However, some male immigration and extra-group males have been observed at least at two sites (Korstjens et al., 2007; Struhsaker, 2010; Colin Chapman and Dennis Twinomugisha, personal communication). In chimpanzees, no case of permanent immigration of (sub)adult males has been observed at any of the several long-term study sites, apart from the immigration of a subadult male at Budongo that followed his mother who immigrated into the same community at an unusually old age a year earlier (Klaus Zuberb€ uhler, Anne Schel, Catherine Hobaiter, personal communication). Finally, in the two long-term studies of bonobos, two new adult males stayed in the Lomako study community for 12 months (Hohmann, 2001), and two males probably immigrated at Wamba during the absence of researchers due to war and during unusual circumstances, such as the disappearance of neighboring groups (Hashimoto et al., 2008; Furuichi, 2011). Thus, there is suggestive evidence of at least a low degree of male-mediated gene flow in many other primates long thought to be characterized by male philopatry. Demographic conditions are known to shape usual and unusual dispersal patterns (Clarke and Glander 2008; Strier, 2008; Kappeler and Watts, 2012). One factor that may play a critical role in male immigration in typically male-philopatric species, such as spider monkeys, is the number of community males. This number could affect immigration in two ways: by providing surplus males, and therefore potentially immigrating males, and by creating situations that facilitate successful immigration. When there are many adult males in a community, for example, risky cooperative enterprises are possible, such as raids into neighboring communities’ territories (Aureli et al., 2006; Wallace, 2008). However, a large number of males also increase competition for limited resources, such as access to ovulating females, possibly leading to ostracism of weaker competitors or of males who are less 7 effective coalition partners. For example, the two peripheral extra-community subadult males we observed in 2003–2004, and the lone extra-community males we encountered in 2003 and 2005, may be examples of ostracism leading to male dispersal from the natal community (this may also have happened to the original resident adult and juvenile males). Attempting to disperse may be a better option for ostracized males than risking the sometimes lethal consequences of coalitionary attacks from more established resident males (Campbell, 2006; Valero et al., 2006; Vick, 2008). Such males, in turn, may become potential immigrants into a new community. Dispersal and killing of community males, however, may have detrimental consequences if the number of adult males decreases below a “safe” threshold. Communities containing only a small number of resident males might be vulnerable to immigration and take-over by extra-community males who may be attracted by a high female-to-male adult sex ratio in such communities. This situation may facilitate successful male immigration and possibly community take-over (Fig. 3). Reports on other species provide support for the series of events hypothesized above that may lead to or allow successful male immigration (Fig. 3). For example, Di Fiore et al. (2009) suggested that the loss of some males from one group of white-bellied spider monkeys, perhaps due to hunting, may have created opportunities for new males to immigrate. Similarly, Korstjens et al. (2007) noted that an adult male transferred permanently into a group of Western red colobus at a time when three of the resident males had disappeared. In that population, too, extra-group males are suspected to be exiles from their natal group who are not yet able to immigrate into a new group (Korstjens et al., 2007). For the chimpanzee community at Bossou, apart from the possible emigration of several natal males who disappeared, researchers observed the temporary appearance of unknown males Fig. 3. Events that may facilitate successful male immigration and possible community takeover. The ovals represent the community. Males in white belong to the community; males in black are extra-community males. After a period in the community immigrating males become community males. This change is depicted in the color change of males (from black to white) and the dashed arrow between “Takeover” and “Recruitment of natal males”. American Journal of Physical Anthropology 8 F. AURELI ET AL. only when there was just a single adult male present (Sugiyama, 1999). Similarly, in bonobos, extra-community males appeared at a time when the number of adult resident males was lower and the female-to-male adult sex ratio was higher than in previous years (Hohmann, 2001). Together, these reports and our observations suggest the same scenario: given that male immigration and community take-over are probably risky prospects in malephilopatric groups, they are expected to occur only under particular circumstances, such as when resident males are few and several extra-community males are available (Fig. 3). That is why male immigration likely occurs only rarely in species typically characterized by female dispersal and male philopatry. The unusual male social dynamics reported in this study fit well within the changing view of male–male cooperation and competition in spider monkeys (cf. Aureli and Schaffner, 2008). Male–male social relationships within the same community appear as the strongest because of the highest levels of affiliation (Fedigan and Baxter, 1984; van Roosmalen and Klein, 1988; Symington, 1990; Slater et al., 2009) and because of males’ cooperation with one another in dangerous activities associated with between-community interactions, such as border patrols and raids (Aureli et al., 2006; Wallace, 2008). However, at some level philopatric males are also rivals in within-community competition, despite sometimes being closely-related to one another, and interactions between males, especially between younger and older males, can be risky and may have lethal consequences (Campbell, 2006; Valero et al., 2006; Vick, 2008; Rebecchini et al., 2011; Schaffner et al., 2012). Our findings do not indicate the need of a paradigm shift in thinking about male philopatry in spider monkeys because male immigration still seems to be exceptional. Nonetheless, our observations suggest that male immigration may occur consistently under certain demographic circumstances (Di Fiore et al., 2009), reflecting the risky nature of male–male relationships. In addition to flexible subgroup composition through a high degree of fission–fusion dynamics, spider monkeys may manifest more flexible dispersal patterns and related population genetics (cf. Di Fiore, 2009) than previously suspected. Thus, our study contributes to a view of greater flexibility in the spider monkey social system than previously believed, which may have implications for other species that are typically considered malephilopatric. ACKNOWLEDGMENTS  The authors thank all the staff from the Area de Conservacion Guanacaste, especially Roger Blanco and Maria Marta Chavarria. 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