Dispersal among male ring-tailed lemurs (Lemur catta) on St. Catherines Islandкод для вставкиСкачать
American Journal of Primatology 70:650–660 (2008) RESEARCH ARTICLE Dispersal Among Male Ring-Tailed Lemurs (Lemur catta) on St. Catherines Island J. A. PARGA1 AND R. G. LESSNAU2,3 1 Department of Social Sciences, University of Toronto at Scarborough, Scarborough, Ontario, Canada 2 St. Catherines Island Foundation Center, Midway, Georgia 3 Department of Biology, Armstrong Atlantic State University, Savannah, Georgia 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. Am. J. Primatol. 70:650–660, 2008. c 2008 Wiley-Liss, Inc. Key words: male dispersal; intertroop transfer; Lemur catta; inbreeding avoidance INTRODUCTION Dispersal behavior can help maintain genetic variation within populations by causing gene flow [Howard, 1960; Lindburg, 1969]. Several proximate forces can drive dispersal, including competition for resources [Waser, 1985] or increased mating opportunities for individuals who disperse [Dobson, 1982]. Inbreeding avoidance is one commonly noted function of dispersal [Clutton-Brock, 1989; Packer, 1979], although whether dispersal is a specific adaptation to protect against inbreeding depression is debatable [Dobson & Jones, 1985; Moore & Ali, 1984, 1985; Packer, 1985; Pusey, 1987]. Among mammals, male-biased dispersal is more common than female-biased dispersal [Greenwood, 1980, 1983], and the same generally holds true for primates [Pusey & Packer, 1987; Pusey, 1992]. When primate males disperse, transfer decisions can often be influenced by mating opportunities and by the r 2008 Wiley-Liss, Inc. intensity of male–male competition. Males frequently transfer into groups due to the presence of cycling females [e.g., mangabeys, Lophocebus albigena: Olupot and Waser, 2001; baboons, Papio hamadryas: Packer, 1979; Manzolillo, 1986; langurs, Presbytis entellus: Borries, 2000], or transfer into groups having more favorable sex ratios or fewer males than in their previous group of residence [e.g., white-faced capuContract grant sponsors: University of Texas at Austin; US National Science Foundation; Ford Foundation. Correspondence to: J. A. Parga, Department of Social Sciences, University of Toronto at Scarborough, 1265 Military Trail, Scarborough, Ont., Canada M1C 1A4. E-mail: email@example.com Received 26 August 2007; revised 15 February 2008; revision accepted 26 February 2008 DOI 10.1002/ajp.20542 Published online 13 May 2008 in Wiley InterScience (www. interscience.wiley.com). Male Dispersal in Lemur catta / 651 chin, Cebus capucinus: Jack & Fedigan, 2004b; rhesus macaque, Macaca mulatta: Drickamer & Vessey, 1973; baboon, P. hamadryas: Alberts & Altmann, 1995; Henzi et al., 1998]. A recent review by Jack  found much evidence among primates that male secondary, or non-natal, dispersal is driven by intrasexual competition, whereas there is less support for inbreeding avoidance as an explanation for secondary male dispersal. This article analyzes patterns of male dispersal in a group-living prosimian primate across a nine-year period to investigate two frequently suggested ultimate explanations for male dispersal: inbreeding avoidance and intrasexual mating competition [Jack, 2003]. If non-natal male dispersal functions primarily in inbreeding avoidance, males would be expected to disperse from a social group before potential daughters become reproductively mature and would not be expected to transfer back to their natal groups after leaving. Conversely, we evaluated the intrasexual mating competition hypothesis for male non-natal dispersal by specifically testing the following variables for their effects on patterns of male intertroop movement: the number of adult females per group, the number of adult males per group, and group sex ratio. If the intrasexual mating competition hypothesis for male secondary dispersal is to be supported, males should move to groups having greater numbers of females, fewer males, or a more favorable sex ratio (fewer males per female) than their previous group of residence. Because our study population is a nonendemic colony of free-ranging ring-tailed lemurs (Lemur catta) maintained on St. Catherines Island (SCI), USA, we first compared male intertroop movement patterns at this location to data on wild individuals of the species. In the wild, L. catta groups have approximately equal numbers of males and females, and dispersal is typically performed by males [Budnitz & Dainis, 1975; Gould, 1994, 1997, 2006a; Jolly, 1966; Jones, 1983; Koyama et al., 2002; Sauther, 1991; Sauther et al., 1999; Sussman, 1991, 1992]. Male dispersal in this species does not appear to be the result of ‘‘eviction’’ due to intragroup aggression, but instead appears to be voluntary [Gould, 2006a; Sussman, 1991]. Previous work has shown that the lemurs on SCI exhibit species-typical social [Keith-Lucas et al., 1999] and reproductive behavior [Parga, 2003; Parga et al., 2006], but no study has previously analyzed male dispersal patterns at this site. In this study, we considered whether male intertroop movement on SCI is similar to male transfer in the wild with respect to: (1) age at natal dispersal, (2) frequency of male transfer, (3) seasonality of dispersal, and (4) the occurrence of single-male vs. group transfers. We then used these data to evaluate the inbreeding avoidance and intrasexual competition hypotheses for male dispersal. MATERIALS AND METHODS Definitions In this article, an animals’ dispersal behavior is defined as, ‘‘...movements away from its own (or group) home range into another area’’ [Bekoff, 1977; p 715]. Whereas Bekoff’s  definition applies to adults, we apply the term regardless of age, and use dispersal to describe individuals who emigrate from natal and non-natal groups. Dispersal events were those in which males stayed in their new groups for at least one month or more before transferring again. Such movements were consistently recorded across the study. Short-term male extra-troop ‘‘visits’’ (lasting from less than a day to a week in length) were not considered dispersal events due to their short duration and the fact that males returned to the group from which they came. Visits were not consistently recorded during the study, and were not included in the present analyses. Incidentally, no male stayed in a new group for more than one week but less than one month [Lessnau, unpublished data]. Study Site and Study Animals SCI is a largely forested barrier island off the coast of Georgia, USA [Thomas et al., 1978]. A colony of L. catta was started at this site by the Wildlife Conservation Society (WCS) with the release of a founder group of six lemurs in 1985 [Keith-Lucas et al., 1999]. Although most lemurs in the SCI population are descendants of the founder population, several unrelated males have been added throughout the years to increase genetic diversity in the population. This colony was deemed particularly apt for a study of dispersal because all adults wear uniquely colored Telonics radio collars (Mesa, AZ) and can therefore be located via radio-telemetry. Also, because the colony is on an island, animals are unable to transfer out of the research area, a frequent difficulty in wild studies of dispersal. L. catta on SCI forage on naturally occurring vegetation, show group ranging behavior, and have established home range areas [Dierenfeld & McCann, 1999; Keith-Lucas et al., 1999]. The lemurs on SCI show breeding seasonality [Jolly, 1966]; however, due to photoperiodic control [Evans & Goy, 1968; Rasmussen, 1985; Van Horn, 1975; Van Horn & Eaton, 1979], reproduction is shifted approximately 6 months from Madagascar [Parga & Lessnau, 2005]. Each lemur group is provisioned once daily with food (monkey chow, fresh fruits, and/ or vegetables) and water at heated shelter sites that the lemurs are able to enter and exit freely. The composition of each group per study year is shown in Table I. Of the males that have resided in the SCI colony (n 5 87), 70 were born into the colony, and 17 were Am. J. Primatol. 652 / Parga and Lessnau born at other institutions and were released into the island population. At its peak size, the colony was composed of four distinct lemur groups [Parga & Lessnau, 2005]. One of these groups was relocated in October 2002 to a zoo, leaving three troops in the island population. Because relatedness in the population is estimated to be fairly high, colony management occasionally removes individuals to reduce inbreeding. Records of all births and deaths since the colony’s start in 1985 allow for determination of matrilineal relatedness among individuals. In 1997, R.G.L. began keeping daily records on the composition of all lemur groups (including data on male intertroop movement). These records were used in TABLE I. Group Composition in October of Each Year, Showing M:F Sex Ratio, Including All Natal Females and Non-Natal Males Two Years of Age and Older Year Group ] males: ] females 1997 1 2 3 1 2 3 1 2 3 1 2 3 4 1 2 3 4 3:4 1:3 5:4 2:5 3:3 3:5 1:6 2:4 3:6 4:5 1:6 3:8 1:4 4:5 4:7 4:6 1:4 Year Group ] males: ] females 2002 1 2 3 4 2 3 4 2 3 4 2 3 4 5 3:7 4:6 4:6 3:4 4:5 2:8 2:4 2:5 2:5 4:8 2:7 2:6 1:4 2:3 the present analysis along with behavioral observations conducted by J. A. P. across five mating seasons between 2000 and 2004. Data Analysis Analyses included all male dispersal events between August 1997 and July 2005. Only males born in 2003 and earlier were included in the calculation of mean male age at natal dispersal. When comparing the number of males within (and the group sex ratios of) pre- and post-transfer groups, the dispersing male was excluded from both groups. The following non-parametric tests were employed: binomial, w2 goodness of fit, Kolmogorov–Smirnov, and Wilcoxon signed-rank sum. All tests were two-tailed, and the level of significance was set at 0.05. All means are reported with the standard error of the mean (SEM). Statistical tests were performed using Statistica, version 5.5 (Stat Soft Inc., 1999, Tulsa, OK). RESULTS 1998 1999 2000 2001 2003 2004 2005 Fig. 1. Male age at natal dispersal (n 5 17). Am. J. Primatol. Natal Dispersal, Frequency of Transfer, and Group Tenure Duration We recorded a total of 30 transfer events. Approximately half of these (n 5 17) were instances of natal dispersal (Table II). Males transferred out of their natal groups between 1.6 and 3 years of age, with a mean age at natal transfer of 2.270.1 years (Fig. 1). The majority of males (88.2%) left their natal groups before reaching 3 years of age. All remaining males transferred out of their natal group shortly after reaching age 3. Only a single male remained in his natal group beyond age 3, but he was removed from the colony for management purposes at 3.6 years. Adult males (age 2 years and older, n 5 9) transferred between non-natal groups approximately every 3.2 years. Group tenure duration 1 3 3 2 2 2 2 4 4 Rangingb 3 Rangingb Rangingb 2 2 3 4 Seasonality of Male Dispersal – Unknowna No No – Yes Yes Yes Yes No No No No Yes Yes No No – Unknowna No Yes – Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes No 3 2 2 3 3 3 3 3 3 4 2 3 4 4 4 2 2 A peak in both types of male dispersal (natal and non-natal) occurred between the months of March and June, during which time 80% of all transfers took place (Fig. 2). This peak in male dispersal coincides with the peak in births on SCI [Parga & Lessnau, 2005]. Only three male transfers occurred during the breeding season: two in November and one in January (Fig. 2). The two November transfers deserve special mention, as they were facilitated by management intervention in group dynamics. Following an aggressive interaction over an estrous female, two resident adult males of one group became injured and were removed from the group by management and placed within the shelter that serves as the location of daily food provisioning. The injured males were not allowed to free-range with the group for several days. Within 2 days of the captivity of these injured males, two young males (aged 1 and 2 years) immigrated from a neighboring group, and remained in this group for the duration of the breeding season. Not recorded in WCS records. These males transferred to a part of the island where no free-ranging lemur groups reside. b a 02-May-2000 01-Aug-1997 08-Apr-2001 05-Apr-2001 02-Mar-2000 24-Jun-2001 24-Jun-2001 01-Mar-2002 01-Mar-2002 05-Apr-2003 05-Nov-2003 05-May-2003 05-Apr-2003 31-Mar-2005 31-Mar-2005 05-Nov-2003 02-Mar-2004 EK BY MN BR JH RY CH DA LE CL CP WD RI TD GA MX FZ 2.1 2.3 2.1 3.0 2.8 2.3 1.9 1.9 1.9 3.0 2.6 2.1 1.9 2.0 2.0 1.6 1.8 0 Unknowna 1 1 0 1 1 1 1 1 1 1 1 1 1 1 2 None Unknowna KL Subadult male None CH RY LE DA RI MX BY CL GA TD CP BR, ED Do Males Disperse Alone or Together? Date of transfer Age at 1st ] of individuals with whom Identity of male transfer (yrs) this male transferred transfer partner(s) between non-natal transfers was highly variable (range: 0.1–5.8 years; n 5 9; Table III). Male TABLE II. List of Natal Male Transfers Was the transfer partner Was the transfer partner a cohort member? a natal male? Group of origin Group transferred into Male Dispersal in Lemur catta / 653 Males that ‘‘transferred together’’ to a new group traveled to their new group on the same day in pairs or as a triplet (Tables II and III). Whether or not males dispersed alone or with other males was known for 16 of the 17 natal male transfers (Table II). In natal dispersal events, males were significantly more likely to transfer with 1–2 other males than alone (binomial test: n 5 16, x 5 2, P 5 0.0018). In particular, natal males were more likely to disperse with one transfer partner rather than disperse alone or with two other males (goodness of fit: w2 5 16.63, df 5 2, Po0.0003; Fig. 3). In contrast, non-natal transfers were no more likely to involve groups of males than lone males (binomial test: n 5 13, x 5 5, P 5 0.157, NS), and such males were equally likely to disperse alone, or with one or two other males (goodness of fit: w2 5 2.00, df 5 2, Po0.368, NS; Table III). Male age was not the driving force for these trends, because age did not significantly affect whether males transferred alone or with other males (Kolmogorov–Smirnov: n1 5 7, n2 5 22, P40.10, NS). Next, we considered the relatedness of transfer partners. Natal males transferred with a same-aged birth cohort member in 38% of cases, and with an older or younger matrilineally related male in 69% of natal transfers (Table II). In all other instances, natal males transferred with older males whose relatedness to them is unknown. It is possible that some natal males may have transferred with their fathers, as the older male transfer partners were old Am. J. Primatol. 1:3 2:6 1:7 1:3 1:3 N/Ab 1:6 1:8 1:8 3:5 0:4 N/Ab N/Ab Sex ratio of pretransfer group (M:F) 4:5 2:7 1:6 3:7 4:5 2:8 2:8 3:5 3:5 2:4 2:6 2:7 2:7 2 3 2 4 2 Rangingb 2 4 4 2 4 Rangingb Rangingb A striking trend was that no male ever transferred back to his natal group, despite the fact that some males transferred several times during the study period (e.g., male KL transferred four times in eight years: Table III). Six males even traveled beyond the home ranges of the L. catta groups into areas of the island with no lemurs (presumably, in search of lemur groups), which necessitated their removal from the island population by colony management. 3 2 3 2 3 3 3 2 2 4 2 2 2 Intrasexual Competition Hypothesis and Male Dispersal Behavior Am. J. Primatol. c b a Male troop tenure began prior to data collection on troop composition. These males transferred to a part of the island where no free-ranging lemur groups reside. These values do not include transfer partners. MK MN None None KL WD None BR, FZ ED, FZ None None GA TD 5.3 8.1 12 12.1 11.2 8.1 9.9 13 6 3.1 3 2.1 2.2 1 1 0 0 1 1 0 2 2 0 0 1 1 19-Jul-1998 8-Apr-2001 30-Mar-2005 23-Apr-2005 19-Jul-1998 5-May-2003 26-Jan-2001 2-Mar-2004 2-Mar-2004 22-Apr-2003 11-Apr-2000 9-May-2005 9-May-2005 KL KL KL KL MK BY ED ED BR LE JH TD GA Unknowna 2.7 4.1 0.1 4.3 5.8 Unknowna 3.1 2.9 1.1 0.1 0.1 0.1 Date of transfer Duration of troop tenure prior to dispersal (years) ] of individuals Age at this Identity of with whom this transfer (years) male transfer male transferred partner(s) Pre-transfer group Avoidance of Natal Groups as Dispersal Destinations Male TABLE III. List of Non-Natal Male Transfers enough to sire the natal male in question and were in the group at the time of their conception. Post-transfer group Sex ratio of posttransfer group (M:F)c 654 / Parga and Lessnau If intrasexual male mating competition is a driving force for non-natal male dispersal, three variables should be potentially important to male transfer decisions: the number of females per group, the number of males per group, and overall group sex ratio. Although the numbers of adult females (aged 2 years and older) per group did not differ significantly between males’ pre- and post-transfer groups (Wilcoxon: Z 5 0.66, n 5 10, Po0.51, NS), males were more likely to transfer into a group having fewer non-natal males than the group which they left (Wilcoxon: Z 5 2.31, n 5 10, Po0.02). Similarly, the M:F sex ratio of pre- and posttransfer groups differed significantly, with males tending to move into groups having a more favorable sex ratio (fewer non-natal males per adult female) than in pre-transfer groups (Wilcoxon: Z 5 2.09, n 5 10, Po0.037). Interestingly, this relationship is only significant when excluding a male’s transfer partners from the sex ratio of the post-transfer group. If transfer partners were included in the calculation of sex ratio for both groups, the sex ratio did not differ significantly between pre- and posttransfer groups (Wilcoxon: Z 5 1.68, n 5 10, Po0.1, NS); this trend would be expected if transferring males do not ‘‘count’’ their transfer partners when assessing the number of males in a prospective group of entry. DISCUSSION Age at Natal Dispersal On SCI, most males (over 88%) leave their natal groups by the age of 2, with almost all other males leaving at the age of 3. In contrast, only 46% of natal males disperse between the ages of 2 and 3 in Berenty, Madagascar [Koyama et al., 2002]. Males in Beza Mahafaly, Madagascar leave their natal groups even later, between the ages of 3 and 5 [Sussman, 1992]. Berenty’s rich habitat or the history of tourist Male Dispersal in Lemur catta / 655 Fig. 2. Seasonality of male dispersal for natal (n 5 17) and non-natal (n 5 13) transfers on SCI between 1997 and 2005. Male dispersal behavior showed a seasonal peak, which coincided with the birth season at this location. Fig. 3. Natal males were significantly more likely to transfer with one or two other males than alone (binomial test: n 5 16, x 5 2, P 5 0.0018). The majority of natal males dispersed from their natal group with a single transfer partner. In contrast, non-natal transfers were no more likely to involve groups of males than lone males (binomial test: n 5 13, x 5 5, P 5 0.157, NS). The number of transfers of each type is listed above each bar. provisioning at this site [Koyama et al., 2001, 2002] may be the reason for the earlier natal transfer of males from Berenty in comparison with Beza. Even with this variation among wild L. catta males, male natal dispersal is an event that generally occurs earlier on SCI than in the wild. This earlier age at natal dispersal on SCI is likely due to advanced male maturation as a result of provisioning. Sexual maturation is a common correlate of animal dispersal [Baker, 1978; Smale et al., 1997], with the timing of dispersal frequently being controlled by body condition or fat reserves [Dufty & Belthoff, 2001; Smale et al., 1997]. In male Belding’s ground squirrels, for example, experimentally provisioned males disperse at an earlier age than unprovisioned males [Nunes & Holekamp, 1996]. Indeed, female sexual maturation occurs more rapidly on SCI than among wild L. catta. Females on SCI reach primiparity at age 2 [Parga & Lessnau, 2005] earlier than the typical primiparous age for females in Madagascar, which is age 3 in Beza [Sussman, 1991] but which can occasionally occur at age 2 in Berenty [Koyama et al., 2001]. Other factors that may lead to earlier male dispersal on SCI include decreased predation pressure or increased familiarity with neighboring troops. Although lemur predators do exist on SCI [Parga & Lessnau, 2005], young males may be more likely to disperse at an earlier age if there is decreased predation pressure at this site as compared with the wild. Also, because the number of potential groups in which to transfer in the wild far exceeds the numbers of groups available to transferring males on SCI, males in this island colony may be Am. J. Primatol. 656 / Parga and Lessnau more familiar with neighboring groups than are males in Madagascar, and as a result may be more likely to attempt transfers at an earlier age. Troop Tenure Duration: Lack of Support for the Inbreeding Avoidance Hypothesis Considering both natal and non-natal dispersal events, males on SCI transfer between groups about as frequently as do males in Madagascar. Adult males transfer between groups about once every 3.5 years in Beza Mahafaly [Sussman, 1992], once every 3.1 years in Berenty [Koyama et al., 2002], and once every 3.2 years on SCI. The frequency of male transfer on SCI clearly falls well within the species’ range. It is important to note, however, that at all three sites there is a great deal of interindividual variation in male troop tenure length. In Beza Mahafaly, some males remain in groups for many years whereas others transfer almost every year [Gould, 1994, 2006b]. Similarly, in Berenty, male troop tenure ranged between 1 and 7 years [Koyama et al., 2002]. On SCI, male troop tenure was also highly variable. Some males remained in non-natal groups for several years before transferring while others stayed for just weeks before transferring again. Such short tenure lengths have been noted among wild males in Madagascar [Gould, 1994; Jones, 1983; Sauther, 1991; Sussman, 1991, 1992]. Dispersing every few years may help some males produce a more genetically diverse set of offspring across their lifetime [Gladstone, 1979; Williams, 1975]. In order for the inbreeding avoidance hypothesis for male secondary dispersal to be supported, males should transfer from a group before potential daughters become sexually mature [Cheney & Seyfarth, 1983]. For male L. catta who remain in a troop for a very short period of time and then transfer, their departure would occur around the time potential daughters would reach sexual maturity [Sussman, 1992]. However, on SCI, females can mate for the first time at the age of 1, and can have their first infant at age 2 [Parga & Lessnau, 2005]. Consequently, there is much overlap in male troop tenure duration and the attainment of sexual maturity by potential daughters. This finding does not support the inbreeding avoidance hypothesis for secondary male dispersal. Seasonality of Male Dispersal Among seasonally breeding primates with male dispersal, male intertroop movement often occurs during the mating season [e.g., vervet monkeys, Cercopithecus aethiops: Henzi & Lucas, 1980; Cheney, 1983; Hanuman langurs, P. entellus: Borries, 2000; Japanese macaque, M. fuscata: Sprague, 1992; rhesus macaque, M. mulatta: Boelkins & Wilson, 1972]. Instead, among L. catta on SCI, the majority Am. J. Primatol. of male dispersal events on SCI coincided with the birth peak at this site, which occurs from March through June [Parga & Lessnau, 2005]. Only a few instances of male dispersal occurred during the mating season on SCI. This pattern is most similar to Berenty, Madagascar, where male dispersal primarily occurs during the birth season [Budnitz & Dainis, 1975; Jones, 1983]. Studies of male transfer in L. catta (including temporary male visits) conducted at Beza Mahafaly have shown that transfer can also occur in the months before and during the mating season, and the birth and lactation seasons [Gould, 1994, 1997, 2006a; Sauther, 1991; Sussman, 1991, 1992]. Therefore, although the overall seasonality of male transfer behavior on SCI is most similar to that described in Berenty [Budnitz & Dainis, 1975; Jones, 1983], the mating season transfers on SCI are also within the range documented for wild L. catta males. A potential adaptive explanation for why male dispersal events occur during the birth season at some locations is that this pattern of dispersal provides opportunities for males to commit infanticide of other male’s offspring [Pereira & Weiss, 1991; van Schaik, 1996]. Male L. catta attacks on infants have been observed at Berenty [Hood, 1994; Ichino, 2005; Jolly et al., 2000], and in captivity at the Duke Lemur Center [formerly, the Duke University Primate Center; Jolly et al., 2000; Pereira & Weiss, 1991]. However, infanticide as an adaptive male strategy in this species has been questioned for several reasons [Sauther et al., 1999; Sussman, 1999]. Because infanticide by males has not been observed on SCI [Parga & Lessnau, 2005], we conclude that there is no direct support from our study location at present to suggest that male dispersal is functionally related to opportunities for infanticide. Instead, it appears that males on SCI transfer primarily during the birth season (when no female is sexually receptive) because they are apt to receive lower levels of aggression from resident group males at this time. The occurrence of two young males transferring into a group during the mating season only after the two injured adult resident males had been enclosed in the group’s shelter provides anecdotal but supporting evidence for this idea. In fact, these two males were the only individuals to ever transfer during the first estrus cycle of the mating season, which takes place during OctoberNovember annually on SCI [Parga & Lessnau, 2005], when rates of aggression among males are extremely high, especially on days of estrus [Parga, 2006]. The only other male who was observed to transfer during the mating season entered a group having a single resident adult male, and entered late in the breeding season (during January). Hence, the birth season appears to be an optimal time for males to disperse, as it likely minimizes the amount of aggression Male Dispersal in Lemur catta / 657 received from resident males of the group they are attempting to join. The proximate mechanism stimulating males to transfer during the birth season is unknown. Also unknown is why male L. catta on SCI do not transfer more frequently during the mating season and accept the cost of aggression from resident males during this time, as do males of other primate species [e.g., vervet monkeys, C. aethiops: Henzi & Lucas, 1980], including wild L. catta males in Beza Mahafaly [Sauther, 1991; Sussman, 1992]. Males in this study did emigrate voluntarily, however, and were not aggressively evicted by any resident group members [Parga, personal observation], which is also the case among wild L. catta [Gould, 2006a; Sussman, 1991]. Males Dispersing Together Vs. Alone: Functional Explanations Males in this study frequently transferred between groups in pairs or triplets. Less than onequarter of transfers were performed by lone males. Natal males in particular were more likely to transfer between groups with at least one other male than alone. Wild L. catta males also tend to transfer in pairs or triplets [Budnitz & Dainis, 1975; Gould, 1994, 1997, 2006a; Jones, 1983; Sussman, 1991, 1992], as do males of several other primate species [e.g., vervets, C. aethiops: Henzi & Lucas, 1980; Japanese macaques, M fuscata: Sugiyama, 1976; long-tailed macaques, M. fascicularis: van Noordwijk & van Schaik, 1985, 2001; de Ruiter & Geffen, 1998; rhesus macaques, M. mulatta: Drickamer and Vessey, 1973; squirrel monkeys, Saimiri sciureus: Mitchell, 1994]. Transferring with a partner can be highly adaptive, as the partner (or partners) can help provide protection against predators or against aggression from resident individuals of the group the males are attempting to enter [i.e., capuchin monkeys, Cebus capucinus: Jack & Fedigan, 2004a,b; vervet monkeys, C. aethiops: Cheney, 1983, Cheney & Seyfarth, 1983]. Transferring L. catta males in the wild receive aggression from resident individuals in the troop that they are attempting to join, and a transfer partner can help males to spot impending attacks from these individuals or from predators [Gould, 1994, 1997, 2006a; Sussman, 1992]. Similarly, males on SCI must also contend with aggression from members of the group they are attempting to join [Parga, unpublished data], and risk attack from a number of potential lemur predators, both aerial and terrestrial [Keith-Lucas et al., 1999; Parga & Lessnau, 2005]. Therefore, as previously suggested by Sussman  and Gould [1994, 1997, 2006a], the strategy of transferring with other males may provide L. catta males with a much safer passage than transferring alone. Transferring into groups with related males may also be functionally related to kin selection [Meikle & Vessey, 1981]. In this study, several groups of males transferring together were known to be closely related through matrilineal lines. Males frequently dispersed out of their natal groups with same-year birth cohort members or with other males born into their natal group who were close in age. Some younger natal males may have also transferred out of their natal groups with their fathers, as the older males with whom they transferred were in the troop when the natal male was conceived, and were also old enough to have fathered them. This speculative idea must await the completion of paternity analyses currently in progress to be properly evaluated. Regardless of relatedness, travelling with an older male may be particularly important because the experience of the older male can aid the successful integration of a younger male into a new social group [Gould, 1994]. A transfer partner (or partners) can also provide dispersing males with valuable affiliative relationships while they are making the transition from one group to another [Gould, 1994, 1997, 2006a]. Indeed, male transfer partners on SCI have been observed mutual grooming and huddling together during resting periods while on the periphery of a new group [Parga, personal observation]. Avoidance of Natal Groups as Dispersal Destinations Notably, no male ever returned to his natal group, despite the fact that some males transferred several times during the study period. This is similar to other cases in which males rarely or never return to their natal group to breed [e.g., capuchins, Cebus capucinus: Jack & Fedigan, 2004b; baboons, P. hamadryas, Packer, 1979; macaques, Macaca spp.: Dittus, 1979; Sugiyama, 1976; Drickamer & Vessey, 1973]. This pattern of avoidance of returning to the natal group is even more striking when one considers the small number of lemur groups on SCI (3–4 throughout much of the colony’s history). As a consequence, the degree of inbreeding on SCI is likely to be lower than it otherwise would be if males did not avoid their natal groups as transfer destinations. Intrasexual Competition Hypothesis: Group Composition and Male Dispersal If male–male competition drives secondary male dispersal, non-natal males might be expected to transfer into groups with greater numbers of females, or groups having more favorable sex ratios than their previous group of residence [e.g., whitefaced capuchin, Cebus capucinus: Jack & Fedigan, 2004b; rhesus macaque, M. mulatta: Drickamer & Vessey, 1973; baboon, P. hamadryas: Packer, 1979; Am. J. Primatol. 658 / Parga and Lessnau Alberts & Altmann, 1995]. Among wild L. catta males in Beza Mahafaly, Madagascar, Sussman  found that males were more likely to leave groups with higher male-to-female sex ratios. In this study, there was not a significant difference in males’ pre- and post-transfer groups in the numbers of adult females. Neither was there a difference in the sex ratio of males’ pre- and post-transfer groups when a male’s transfer partners were included in the calculation of sex ratio (for both pre- and posttransfer groups). However, group sex ratios were found to differ significantly between males’ pre- and post-transfer groups when males’ transfer partners were excluded from the post-transfer group-male count. We interpret this as support for the intrasexual mating competition hypothesis for secondary male dispersal. Furthermore, these findings suggest that transferring males do not include current transfer partners when assessing the composition of a prospective group of entry. We also found that male L. catta on SCI were significantly more likely to join a group having fewer non-natal males than in their previous group. This trend was noted among wild L. catta in Berenty, Madagascar, and was interpreted as male avoidance of groups with a greater number of potential competitors [Jones, 1983]. The number of males per group is indicative of the amount of competition a male will likely experience because females commonly mate with multiple males during estrus, and male dominance rank shows much instability at this time [Gould, 1994, 1997; Jolly, 1966; Koyama, 1988; Sauther, 1991; Taylor & Sussman, 1985]. There is also a strong positive correlation between the number of male mates per female and the rate of male–male aggression during estrus [Parga, 2006]. Furthermore, after male transfers have occurred during the spring and summer months on SCI, troop composition tends to remain stable until the fall mating season. Thus, secondary male dispersal in L. catta (dispersal between two non-natal groups) appears to be driven by avoidance of the natal group as a transfer destination, as well as by avoidance of groups in which a male would experience more intense male–male competition during the mating season. ACKNOWLEDGMENTS We thank the SCI Foundation and the WCS for their maintenance of the L. catta colony throughout the years. L. Gould, P. Henzi, R. R. Lawler, R. J. Lewis, D. J. Overdorff, L. Shapiro, and one anonymous reviewer kindly provided comments that greatly improved this article. A. Henry helped compile records on male intertroop movement and S.J. Lozano aided in figure formatting. During the writing of this paper, J. A. Parga was supported by a Ford Foundation Dissertation Fellowship and by a US National Science Foundation Postdoctoral Am. J. Primatol. Fellowship. All research reported in this article adhered to the American Society of Primatologists’ Principles for the Ethical Treatment of Non Human Primates, was approved by both the WCS and the IACUC at the University of Texas at Austin, and adhered to the legal requirements of the United States. REFERENCES Alberts SC, Altmann J. 1995. Balancing costs and opportunities: dispersal in male baboons. Am Nat 145:279–306. Baker RR. 1978. The evolutionary ecology of animal migration. New York: Holmes & Meier Publishers. 1012 p. Bekoff M. 1977. Mammalian dispersal and the ontogeny of individual behavioral phenotypes. Am Nat 111:715–732. Boelkins RC, Wilson AP. 1972. Intergroup social dynamics of the Cayo Santiago rhesus (Macaca mulatta) with special reference to changes in group membership by males. Primates 13:125–140. Borries C. 2000. Male dispersal and mating season influxes in Hanuman langurs living in multi-male groups. In: Kappeler PM, editor. Primate males: causes and consequences of variation in group composition. Cambridge: Cambridge University Press. p 146–158. Budnitz N, Dainis K. 1975. Lemur catta: ecology and behavior. In: Tattersall I, Sussman RW, editors. Lemur biology. New York: Plenum Press. p 219–235. Cheney DL. 1983. Proximate and ultimate factors related to the distribution of male migration. In: Hinde RA, editor. Primate social relationships: an integrated approach. Oxford: Blackwell Scientific Publications. p 241–249. Cheney DL, Seyfarth RM. 1983. Nonrandom dispersal in freeranging vervet monkeys: social and genetic consequences. Am Nat 122:392–412. Clutton-Brock TH. 1989. Female transfer and inbreeding avoidance in social mammals. Nature 337:70–72. de Ruiter JR, Geffen E. 1998. Relatedness of matrilines, dispersing males and social groups in long-tailed macaques (Macaca fascicularis). Proc R Soc Lond B 265:79–87. Dierenfeld ES, McCann CM. 1999. Nutrient composition of selected plant species consumed by semi free-ranging liontailed macaques (Macaca silenus) and ringtailed lemurs (Lemur catta) on St. Catharines Island, Georgia, USA. Zoo Biol 18:481–494. Dittus WPJ. 1979. The evolution of behaviors regulating density and age-specific sex ratios in a primate population. Behaviour 69:263–302. Dobson FS. 1982. Competition for mates and predominant juvenile male dispersal in mammals. Anim Behav 30:1183–1192. Dobson FS, Jones WT. 1985. Multiple causes of dispersal. Am Nat 126:855–858. Drickamer LC, Vessey S. 1973. Group changing in freeranging male rhesus monkeys. Primates 14:359–368. Dufty Jr AM, Belthoff JR. 2001. Proximate mechanism of natal dispersal: the role of body condition and hormones. In: Clobert J, Danchin E, Dhondt AA, Nichols JD, editors. Dispersal. Oxford: Oxford University Press. p 215–229. Evans CS, Goy RW. 1968. Social behaviour and reproductive cycles in captive ring-tailed lemurs (Lemur catta). J Zool 156:181–197. Gladstone DE. 1979. Promiscuity in monogamous colonial birds. Am Nat 114:545–557. Gould L. 1994. Patterns of affiliative behavior in adult male ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve, Madagascar [dissertation]. St. Louis (MO): Washington University. 268 p. Available from: University Microfilms, Ann Arbor, MI; AAT 9509913. Male Dispersal in Lemur catta / 659 Gould L. 1997. Intermale affiliative behavior in ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve, Madagascar. Primates 38:15–30. Gould L. 2006a. Male sociality and integration during the dispersal process in Lemur catta: a case study. In: Jolly A, Sussman RW, Koyama N, Rasamimanana H, editors. Ringtailed lemur biology: Lemur catta in Madagascar. New York: Springer Science1Business Media. p 296–310. Gould L. 2006b. Lemur catta ecology: what we know and what we need to know. In: Gould L, Sauther ML, editors. Lemurs: ecology and adaptation. New York: Springer Science1 Business Media. p 255–274. Greenwood PJ. 1980. Mating systems, philopatry, and dispersal in birds and mammals. Anim Behav 28:1140–1162. Greenwood PJ. 1983. Mating systems and the evolutionary consequences of dispersal. In: Swingland, IR, Greenwood PJ, editors. The ecology of animal movement. Oxford: Clarendon Press. p 116–131. Henzi SP, Lucas JW. 1980. Observations on the inter-troop movement of adult vervet monkeys (Cercopithecus aethiops). Folia Primatol 33:220–235. Henzi SP, Lycett JE, Weingrill T. 1998. Mate guarding and risk assessment by male mountain baboons during intertroop encounters. Anim Behav 55:1421–1428. Hood LC. 1994. Infanticide among ringtailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. Am J Primatol 33:65–69. Howard WE. 1960. Innate and environmental dispersal of individual vertebrates. Am Midland Nat 63:152–161. Ichino S. 2005. Attacks on a wild infant ring-tailed lemur (Lemur catta) by immigrant males at Berenty, Madagascar: interpreting infanticide by males. Am J Primatol 67: 267–272. Jack K. 2003. Males on the move: evolutionary explanations of secondary dispersal by male primates. Primate Rep 67: 61–83. Jack KM, Fedigan L. 2004a. Male dispersal patterns in whitefaced capuchins, Cebus capucinus. Part 1: patterns and causes of natal emigration. Anim Behav 67:761–769. Jack KM, Fedigan L. 2004b. Male dispersal patterns in white-faced capuchins, Cebus capucinus. Part 2: patterns and causes of secondary dispersal. Animal Behav 67: 771–782. Jolly A. 1966. Lemur behavior. Chicago: University of Chicago Press. 187p. Jolly A, Caless S, Cavigelli S, Gould L, Pereira ME, Pitts A, Pride RE, Rabenandrasana HD, Walker JD, Zafison T. 2000. Infant killing, wounding and predation in Eulemur and Lemur. Int J Primatol 21:21–40. Jones KC. 1983. Inter-troop transfer of Lemur catta males at Berenty, Madagascar. Folia Primatol 40:145–160. Keith-Lucas T, White FJ, Keith-Lucas L, Vick LG. 1999. Changes in behavior in free-ranging Lemur catta following release in a natural habitat. Am J Primatol 47:15–28. Koyama N. 1988. Mating behavior of ring-tailed lemurs (Lemur catta) at Berenty, Madagascar. Primates 29: 163–175. Koyama N, Nakamichi M, Oda R, Miyamoto N, Ichino S, Takahata Y. 2001. A ten-year summary of reproductive parameters for ring-tailed lemurs at Berenty, Madagascar. Primates 42:1–14. Koyama N, Nakamichi M, Ichino S, Takahata Y. 2002. Population and social dynamics changes in ring-tailed lemur troops at Berenty, Madagascar between 1989–1999. Primates 43:291–314. Lindburg DG. 1969. Rhesus monkeys: mating season mobility of adult males. Science 166:1176–1178. Manzolillo DL. 1986. Factors affecting intertroop transfer by adult male Papio anubis. In: Else JG, Lee PC, editors. Primate ontogeny, cognition and social behaviour. Cambridge: Cambridge University Press. p 371–380. Meikle DB, Vessey SH. 1981. Nepotism among rhesus monkey brothers. Nature 294:160. Mitchell CL. 1994. Migration alliances and coalitions among adult male South American squirrel monkeys (Saimiri sciureus). Behaviour 130:169–190. Moore J, Ali R. 1984. Are dispersal and inbreeding avoidance related? Anim Behav 32:94–112. Moore J, Ali R. 1985. Inbreeding and dispersal—reply to Packer (1985). Anim Behav 33:1367–1369. Nunes S, Holekamp KE. 1996. Mass and fat influence the timing of natal dispersal in Belding’s ground squirrels. J Mammal 77:807–817. Olupot W, Waser PM. 2001. Correlates of intergroup transfer in male grey-cheeked mangabeys. Int J Primatol 22: 169–187. Packer C. 1979. Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim Behav 27:1–36. Packer C. 1985. Dispersal and inbreeding avoidance. Anim Behav 33:676–678. Parga JA. 2003. Copulatory plug displacement evidences sperm competition in Lemur catta. Int J Primatol 24: 889–899. Parga JA. 2006. Male mate choice in Lemur catta. Int J Primatol 27:107–131. Parga JA, Lessnau RG. 2005. Female age-specific reproductive rates, birth seasonality, and infant mortality of ring-tailed lemurs on St. Catherines Island: 17-year reproductive history of a free-ranging colony. Zoo Biol 24:295–309. Parga JA, Maga M, Overdorff DJ. 2006. High-resolution X-ray computed tomography scanning of primate copulatory plugs. Am J Phys Anthropol 129:567–576. Pereira ME, Weiss ML. 1991. Female mate choice, male migration, and the threat of infanticide in ringtailed lemurs. Behav Ecol Sociobiol 28:141–152. Pusey AE. 1987. Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol Evol 2: 295–299. Pusey AE. 1992. The primate perspective on dispersal. In: Stenseth NC, Lidicker Jr WZ, editors. Animal dispersal: small mammals as a model. London: Chapman & Hall. p 243–259. Pusey AE, Packer C. 1987. Dispersal and philopatry. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: University of Chicago Press. p 250–266. Rasmussen DT. 1985. A comparative study of breeding seasonality and litter size in eleven taxa of captive lemurs (Lemur and Varecia). Int J Primatol 6:501–517. Sauther ML. 1991. Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Am J Phys Anthropol 84:463–477. Sauther ML, Sussman RW, Gould L. 1999. The socioecology of the ringtailed lemur: thirty-five years of research. Evol Anthropol 8:120–132. Smale L, Nunes S, Holekamp KE. 1997. Sexually dimorphic dispersal in mammals: patterns, causes, and consequences. Adv Study Behav 26:181–250. Sprague DS. 1992. Life history and male intertroop mobility among Japanese macaques (Macaca fuscata). Int J Primatol 13:437–454. Sugiyama Y. 1976. Life history of male Japanese monkeys. Adv Study Behav 7:255–284. Sussman RW. 1991. Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. Am J Phys Anthropol 84:43–58. Sussman RW. 1992. Male life history and intergroup mobility among ringtailed lemurs (Lemur catta). Int J Primatol 13:395–413. Sussman RW. 1999. Primate ecology and social structure, lorises, lemurs and tarsiers. Vol. 1. Needham Heights: Pearson Custom Publishing. 284p. Am. J. Primatol. 660 / Parga and Lessnau Taylor L, Sussman RW. 1985. A preliminary study of kinship and social organization in a semi-free-ranging group of Lemur catta. Int J Primatol 6:601–614. Thomas DH, Jones GD, Durham RS, Larsen CS. 1978. The anthropology of St. Catherines Island. 1. Natural and cultural history. Anthropol Pap Am Mus Nat Hist 55:157–248. Van Horn RN. 1975. Primate breeding season: photoperiodic regulation in captive Lemur catta. Folia Primatol 24:203–220. Van Horn RN, Eaton GG. 1979. Reproductive physiology and behavior in prosimians. In: Doyle GA, Martin RD, editors. The study of prosimian behavior. New York: Academic Press. p 111–122. Am. J. Primatol. van Noordwijk MA, van Schaik CP. 1985. Male migration and rank acquisition in wild long-tail macaques (Macaca fascicularis). Anim Behav 33:849–861. van Noordwijk MA, van Schaik CP. 2001. Career moves: transfer and rank challenge decisions by male long-tailed macaques. Behaviour 138:359–395. van Schaik CP. 1996. Social evolution in primates: the role of ecological factors and male behaviour. Proc Br Acad 88: 9–31. Waser PM. 1985. Does competition drive dispersal? Ecology 66:1170–1175. Williams GC. 1975. Sex and evolution. New Jersey: Princeton University Press. 200p.