- Email: [email protected]
Mate competition and reproductive correlates of female dispersal in a polygynous primate species (Rhinopithecus roxellana)
Behavioural Processes 79 (2008) 165–170
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Mate competition and reproductive correlates of female dispersal in a polygynous primate species (Rhinopithecus roxellana) Dapeng Zhao a , Weihong Ji b , Baoguo Li a,∗ , Kunio Watanabe c a
College of Life Sciences, Northwest University, Xi’an, China Institute of Natural Resources, Massey University, Auckland, New Zealand c Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan b
a r t i c l e
i n f o
Article history: Received 27 March 2008 Received in revised form 9 July 2008 Accepted 13 July 2008 Keywords: Female dispersal Mate competition Polygynous Reproductive output Sichuan snub-nosed monkeys
a b s t r a c t Different mating systems in group-living animals have characteristic behavioral correlates that are primarily related to mate competition. Mate competition may push individuals to selectively make dispersal decisions for the purpose of maximizing of opportunities for reproduction. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is a polygynous primate species endemic to China. We provide the first data on female dispersal in a free-ranging group of R. roxellana in the Zhouzhi National Nature Reserve, Qinling Mountains, China. Both adult and subadult female dispersal occurred. Immigration/emigration rates of adult females are higher than those of subadult females. Mate competition is one apparent driving force behind adult female dispersal, and inbreeding avoidance is the possible proximate factor influencing subadult female dispersal. Adult female R. roxellana employ various reproductive strategies related to dispersal, which may increase their reproductive success. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Groups of many animal species contain adults of both sexes. Based on current socioecological theory, the mating system of a species or population is determined by the spatial and temporal distribution of adult males and receptive females, i.e. their social organization (Davies, 1991; Reynolds, 1996). Different mating systems, especially in primate species, have characteristic behavioral correlates that are primarily related to mate competition in the same sex (e.g., Kappeler, 1997). For instance, mate competition may push individuals to selectively transfer between groups for the purpose of maximization of their reproduction (e.g., Cetacea: Tursiops aduncus, Möller and Beheregaray, 2004; Chiroptera: Nyctalus noctula, Petit et al., 2001; Perissodactyla: Equus caballus, Monard and Duncan, 1996; Primates: Hylobates lar, Brockelman et al., 1998). Primate societies are characterized by high rates of dispersal of individuals (Greenwood, 1980; Pusey, 1992). In a large number of primate species, males tend to disperse more than females; in other species, however, both sexes disperse, or dispersal is femalebiased (Pusey and Packer, 1987; Isbell and van Vuren, 1996). The proximate causes of primate dispersal, which obviously differ in
∗ Corresponding author at: College of Life Sciences, Northwest University, North TaibaiRoad No. 229, Xi’an, Shaanxi Province 710069, China. Tel.: +86 29 88302048; fax: +86 29 88303572. E-mail addresses: [email protected] (D. Zhao), [email protected] (B. Li). 0376-6357/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2008.07.006
different species and among individuals of different age/sex classes within the same species, may include mate competition, mate choice, resource competition and inbreeding avoidance (Clobert et al., 2001; Lawson Handley and Perrin, 2007). For Old World monkey species, male-biased dispersal has been well documented, as have certain notable exceptions, including hamadryas baboons, red colobus and black colobus (Pusey and Packer, 1987): female transfers are very rare in Old World monkeys (Moore, 1984), but do occur in some langur species (Procolobus badius: Marsh, 1979; Trachypithecus phayrei: Borries et al., 2004; Presbytis thomasi: Sterck et al., 2005). Darwin’s theory of sexual selection is expressed, within groups, both in direct competition between members of the same sex and in the mating preferences of one sex for the other (Paul, 2002). In primate research, female mate competition over males is especially important in polygynous species, although male–male competition for mates and female mate choice are both common (Smuts, 1987). The Sichuan snub-nosed monkey (Rhinopithecus roxellana), a strict seasonal breeder, is a polygynous colobine species; its basic social and reproductive unit is the one-male unit (OMU), which consists of a single resident male, a number of adult females, subadult females, juveniles and infants (Chen et al., 1983; Li and Zhao, 2007). It has been suggested that sexual competition in this polygynous species may have a skewed representation: females faced with multiple competitors will exhibit a high level of sexual competition, i.e. female mate competition, while the single resident male will not experience within-unit sexual competition.
166
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170
Female R. roxellana strives for greater copulation access to the sole resident male by behavioral strategies such as sexual interference (Li and Zhao, 2007). To date, research on individual dispersal in R. roxellana is still in its infancy, and so far has focused on male dispersal, which generally occurs when an OMU’s young males reach about 4 years of age or when the adult male is replaced by another male from an all-male group (Chen et al., 1983). No systematic reports have been published on female dispersal or factors influencing it. Here, we present the first data on female dispersal and individual reproductive output in a free-ranging group of R. roxellana where all members are individually recognized according to their physical characteristics. Data are from long-term records accumulated at Zhouzhi National Nature Reserve in the Qinling Mountains, China. The main purpose of this paper is to investigate whether both adult female dispersal (breeding dispersal) and subadult female dispersal (natal dispersal) occur in this species, to explore whether mate competition drives female dispersal, and to discuss female reproductive strategies behind this behavior. 2. Methods
(a) Adult female: No less than 5 years, about half the body size of adult males. The golden guard hairs in the cape area were much shorter than those of adult males. Their breasts and nipples were large and easily seen. (b) Subadult female: Three to four years old, about two-thirds the body size of adult females. They lacked golden guard hairs in the cape and their breasts and nipples were significantly smaller than those of adult females. (c) Infant: Zero months to one year old. Their hair is light brownish gray or light brown, appearing white in sunshine. They are sometimes observed playing with juveniles or other infants, but spend most of their time beside their mothers or sucking milk from adult females. 2.4. Measuring female dispersal In gregarious primates, dispersal refers to a change in group membership (Pusey and Packer, 1987). We also define dispersal as leaving or entering the OMU within the focus group, not necessarily accompanied by a change in range. When dispersal involves a female emigrating from one OMU and immigrating to another OMU within the focal group, we refer to it as female transfer.
2.1. Study site and species 2.5. Data collection This study was carried out in the Zhouzhi National Nature Reserve, which was established in 1985 to protect 52,931 km2 of temperate forest on the northern slopes of the Qinling Mountains, China (Li and Zhao, 2007; Zhao et al., 2008a,b,c,d). The study animals were members of one R. roxellana group, consisting of OMUs that travel together all the day. The focal group, as one open population, is unstable as several OMUs disappeared from or appeared in it; the group size ranged from 61 to 116 individuals during the observation period. 2.2. Food provisioning In October 2001 we began to habituate the focal group. A 15 m × 30 m provisioning site was set up at Sanchakou (1646 m above sea level) in Gongnigou valley (33◦ 48 68 N, 108◦ 16 18 E). The assistants searched for monkeys of the focal group and attracted them to the provisioning site at approximately 9:00 every day when research was being conducted. Artificial factors, such as leading monkeys to the provisioning site by assistants, especially in the early periods, might have influenced the monkeys’ behavior and social activities, but they soon habituated to the provisioning site, so reducing outside influence (Zhao et al., 2008a,b,c,d). Apples, radishes, and corn were provided three times per day, approximately 200 g per monkey per day in total. Compared with the daily total diet of R. roxellana, energy intake from the provisioned food is very limited and thus its influence would on the whole be minimal (Li and Zhao, 2007). After successful habituation, the group could be observed daily. At night, the monkeys’ roosts were ordinarily located within a 3 km radius of the provisioning site. At the end of the observation period, the monkeys were free-living in the region of the west ridge. During the study period we obtained behavioral data from distances between 0.5 and 50 m. 2.3. Individual identification and age class By late November 2001, all members were individually recognized by prominent physical characteristics, such as body size, pelage color, hair patterns, or physical disabilities (Zhao et al., 2005, 2008a,b,c,d). In this study, we focus on two age classes of female monkeys and the infant class, which are defined as follows:
Observations were made from October 2001 to May 2005 (316 observation days, 1736.2 observation hours in total). We recorded changes in group composition and checked the animals during each observation month, especially the first observation week during each study period. For female dispersal events the group of origin and destination were noted if possible, as well as whether the female concerned was subadult or adult, and whether the female was caring or not caring for an infant. The mating season, from late September to early December, and the birth season, from March to May, respectively, were defined according to Li and Zhao (2007). Birth data on the focal group were gathered during each birth season from 2002 to 2006, as described by Zhao et al. (2008b). Furthermore, we recorded agonistic encounters between resident males of different OMUs via the “all occurrences” and “behavioral sampling” methods (Martin and Bateson, 2007). Description of the forms of aggression and submission followed Li et al. (2006). 2.6. Data analysis Unit size refers to weaned individuals only (Table 1). Dependent offspring are not considered to represent effective feeding competitors (Janson and Goldsmith, 1995), based on models in Dunbar (1988), and are generally excluded from the analysis and discussion. Birth rates were measured as actual births/female/year for OMUs of different sizes and for different numbers of females per OMU. Calculation methods were based upon the description by Watts (1990). Within the social structure of R. roxellana, the rank of the OMU is represented by its resident male’s rank (Li et al., 2006). For the dominance of resident males in the focal group, we calculated a dominance index (Zumpe and Michael, 1986). This index, expressed as a percentage, is based on the number and direction of aggressive and submissive behaviors exchanged among resident males, as described in detail by Li et al. (2006). In this paper, changes in size and composition of groups were similarly treated as independent data points, following Stokes et al. (2003). Different subsets of the same individuals were commonly treated as independent groups (Altmann and Altmann, 1977). Statistical analyses were conducted in SPSS 12.0. All tests were two-tailed and the results were considered significant at p < 0.05.
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170 Table 1 OMU size and composition of Polygynous Rhinopithecus roxellana Unit ID
Unit composition TOT-I
TOT + I
M/SAF
AF/SAF
BaZiTou ChangMao DuanZhi FangPian HongDian HeiTou JingZiTou LuoPan PengKe TuTou ZhongZhi
9.63 9.86 7.90 7.50 11.86 7.75 8.38 15.4 5.00 7.75 5.00
11.50 11.14 9.40 7.50 14.43 8.63 11.38 20.00 5.75 9.75 5.50
M/AF 0.25 0.30 0.24 0.50 0.19 0.31 0.23 0.14 0.33 0.22 0.50
0.50 0.50 1.67 1.00 0.50 0.88 0.72 0.42 1.00 2.00 0.50
2.00 1.64 7.00 2.00 2.57 2.89 3.18 3.00 3.00 9.00 1.00
n AF 4.00 3.28 4.20 2.00 5.14 3.25 4.38 7.20 3.00 4.50 2.00
n SAF 2.00 2.00 0.60 1.00 2.00 1.13 1.38 2.40 1.00 0.50 2.00
Mean ±S.D.
8.73 ±2.97
10.45 ±4.12
0.29 ±0.12
0.88 ±0.52
3.84 ±2.59
3.92 ±1.48
1.33 ±0.67
Note: For those units within the focal group we use one count per observation month and then calculated the median. TOT-I = the whole group size excluding infants; TOT + I = the whole group size including infants; M/AF = the resident male–adult females ratio; M/SAF = the resident male–subadult females ratio; AF/SAF = adult females–subadult females ratio; n AF = numbers of adult females in the unit; n SAF = numbers of subadult females in the unit.
3. Results A total of 20 immigration and 17 emigration events (Fig. 1) was recorded involving 21 adult females (80.77%) and 5 subadult females (19.23%). It includes 11 transfers between known units, i.e. inter-unit female transfer (8 adult females, 72.73% and 3 subadult females, 27.27%), with the remainder consisting of 6 emigrations
167
from and 9 immigrations into the focal group. 17 adult females and 3 subadult females immigrated (1 immigration every 0.21 adult female years, 1 immigration every 0.83 subadult female years). 12 adult females and 5 subadult females emigrated (1 emigration every 0.30 adult female years, 1 emigration every 0.72 subadult female years). We found that there was no female who dispersed more than once in this study. All adult female transfers occurred in the interval between the birth season and mating season (birth season–mating season interval (June to early September): 51.74%; mating season–birth season interval (middle December to February): 48.26%). Subadult female transfers mainly took place in the interval between the mating season and birth season and also occurred in the early mating season (birth season–mating season interval: 50.00%; mating season–birth season interval: 25.00%; early mating season: 25.00%). 3.1. Dispersal in relation to unit size and intra-unit female number For 11 cases of female transfer between known OMUs of the focal group, adult females were found to transfer into significantly smaller OMUs (Wilcoxon signed ranks test: n = 8, Z = −2.565, p = 0.010). This finding did not apply to subadult females (n = 3, Z = −1.604, p = 0.109). Neither adult females nor subadult females showed significant preferences for OMUs with fewer females (i.e. including adult plus subadult individuals (Wilcoxon signed ranks test: adult females, n = 8, Z = −1.890, p = 0.059 and subadult females, n = 3, Z = −1.342, p = 0.180)). Adult females, however, showed significant preference for OMUs containing fewer adult females (Wilcoxon signed ranks test: n = 8, Z = −2.598, p = 0.009) while
Fig. 1. Female transfer in the focal group. Solid lines indicate all females present were counted. Dotted lines indicate not all female were counted in the focal group. Arrows indicate transfers in and out of the group. A means “adult female”, S means “subadult female”, MT means “male takeover occurred”, MD means “resident male disappeared”, MJ means “a new male joined”. Superscripts: a means “the adult female transfer when she is pregnant”, b means “the adult female transfer with her new infant”, and c means means “the one-male unit joined the focal group”, means “the one-male unit disappeared during the “the adult female transfer after her infant disappeared”; means “the disappearance of the one-male unit was noted after an interruption of observations”. observation”,
168
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170
subadult females did not (n = 3, Z = −1.000, p = 0.317). In addition, subadult females showed no preference for OMUs with fewer subadult females (n = 3, Z = −0.535, p = 0.593). For 15 cases of female dispersal consisting of 6 emigrations out of and 9 immigrations into the focal group, the OMU from which an adult female emigrated, or into which an adult female immigrated, did not differ in mean unit size from the focal group (one-sample ttest: emigration, d.f. = 3, t = −0.676, p = 0.548; immigration, d.f. = 8, t = 0.799, p = 0.447). Similarly, the size of the OMU from which a subadult female emigrated did not differ from the mean size of OMUs within the focal group (d.f. = 1, t = −0.820, p = 0.563). Adult females left or joined an OMU with both a similar total of females (one-sample t-test: emigration, d.f. = 3, t = 0.001, p = 1.000; immigration, d.f. = 8, t = 1.107, p = 0.301) and a similar number of adult females (one-sample t-test: emigration, d.f. = 3, t = 1.320, p = 0.279; immigration, d.f. = 8, t = 1.620, p = 0.144) compared with mean numbers among OMUs in the focal group. Similarly, subadult females emigrate from an OMU with both a similar total of females (one-sample t-test: d.f. = 1, t = 0.750, p = 0.590) and similar total of subadult females (d.f. = 1, t = 0.670, p = 0.624) compared with mean numbers among OMUs in the focal group. 3.2. Dispersal in relation to female reproductive status Female Sichuan snub-nosed monkeys generally give birth every second year (Zhao et al., 2008b). During our study, adult female dispersal could be simply divided into four different categories according to reproductive status: (1) Pregnant females’ transfer: During the mating season–birth season interval, three females (JinGu, LiuLiu, and TieMao) transferred when they were likely to be pregnant (Yan and Jiang, 2006). (2) Lactating females’ transfer: Three adult females (PianFen, BaiXian, and WeiZhiMing) transferred with their newborn infants. The infants survived in their new units. WeiZhiMing gave birth in the first post-immigration birth season while PianFen and BaiXian gave birth in the second post-immigration birth season. (3) One adult female, HeiDian, made an inter-unit transfer after her newborn infant disappeared for unknown reasons. She gave birth in both the following two post-immigration birth seasons. (4) For the remaining other 14 adult females, 6 who moved during the birth season–mating season interval gave birth in the following 2 post-immigration birth seasons (83.33% in the first birth season and 16.67% in the second birth season). There were no births recorded for any of the eight females who immigrated in the mating season–birth season interval during the following two post-immigration birth seasons. All infants born to immigrating females survived. Most of the adult females that emigrated had not given birth during the preceding birth season. Overall, 76.47% of adult females and 66.67% of subadult females experience reproductive success within two post-immigration birth seasons. Birth rate is significantly correlated to both unit size and unit female numbers (Pearson correlation test: unit size, rs = 0.687, p < 0.001; unit female numbers, rs = 0.710, p < 0.001). Conversely, infant survivorship is not significantly correlated with either group size or female group size (Pearson correlation test: unit size, rs = 0.094, p = 0.634; unit female numbers, rs = −0.033, p = 0.866). 3.3. Dispersal in relation to OMU rank In all cases females (adults and subadults) transferred from higher-ranking to lower-ranking OMUs. In all cases the OMUs from
which females emigrated contained a resident male that was sexually active and capable of siring offspring, given the birth data. The phenomenon of male takeover, a form of individual dispersal, has been found in only one case within the focal group. The intruding male, JiaBan, superseded the resident male, HeiTou, and became the new resident male, after which the old resident male, HeiTou, left the focal group on April 28th 2003. During our study period, no female dispersal occurred in this OMU whereas female dispersal prevailed in other OMUs where no male takeover occurred. 4. Discussion To our knowledge, this is the first report of female dispersal in any species of Rhinopithecus. Both adult and subadult female R. roxellana are involved in dispersal activity. Immigration rates and emigration rates of adult females are higher than those of subadult females, which contrasts with the findings of some other colobine studies, such as Nasalis larvatus (Murai et al., 2007). In previous research, it was believed that only male dispersal occurs in R. roxellana (Chen et al., 1983). We report, for the first time, that R. roxellana displays dispersal of both sexes, as in some other colobine species (e.g., Procolobus verus: Korstjens and Schippers, 2003), although to date it could not be identified whether there is female-biased dispersal or male-biased dispersal in this species. The mate competition hypothesis explains dispersal by the sex that competes most over access to reproductive partners (Clobert et al., 2001). As regards inter-unit transfers, adult female R. roxellana tend to transfer into those OMUs with few adult females, which suggests that female mate competition should be involved. Of the major explanations for female dispersal, another that is widely applicable to polygynous primates is the “competitive female choice” model (Altmann et al., 1977), which holds that females are choosing to transfer in order to maximize their reproductive success. For R. roxellana in this study, 76.47% of adult females and 66.67% of subadult females show reproductive success within two post-immigration birth seasons, compared to a low birth rate in the original unit during the birth season preceding immigration. This suggests that females transfer between OMUs because doing so may increase their reproductive success; to some extent supporting the “competitive female choice” model (Altmann et al., 1977). In theory, however, the lactating females that made interunit transfers would be expected to be vulnerable to infanticide, which has been reported in this species under captive conditions (Zhang et al., 1999); this is a question which must be left for future consideration. The timing of dispersal could provide interesting clues to ultimate causes (Lawson Handley and Perrin, 2007). “Extra-group attraction” has been shown to drive emigration in several groupliving primate species such as chimpanzees, macaques, mangabeys, vervets and guenons (Lawson Handley and Perrin, 2007). In this case, the timing of dispersal generally coincides with the mating season. Adult female dispersal in R. roxellana did not take place in the mating season but in the interval between the birth season and the mating season, and adult females who shifted in the birth season–mating season interval gave birth in the following two post-immigration birth seasons. This suggests that the choice of the dispersal period in female R. roxellana is crucial for subsequent reproductive success although extra-group attraction may not be the driving factor for female dispersal in this species. Zhao et al. (2008b) reported that after the male takeover, the new resident male made use of the birth season-mating season interval to establish reproductive relationships. It may thus be inferred that adult females which choose the birth season–mating season interval to disperse may be adopting a similar reproductive strategy.
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170
Though it is hard to confirm, there is an intriguing suggestion that pregnant females emigrate/transfer at a higher than expected rate in some female transfer species (e.g., Cercopithecus ascanius: Haddow, 1952; Alouatta palliata: Jones, 1980). Three such cases were observed in female R. roxellana, where pregnant females chose the mating season–birth season interval to transfer into smaller units. This suggests that pregnant females may avoid feeding competition within the resident unit and ensure that their coming offspring will have better food resources in a new unit. In addition, some female transfers in primates (e.g., gorillas and chacma baboons) followed reproductive failure, i.e. death of the infant (Harcourt, 1978). In this study, one similar event occurred. It is possible that female R. roxellana may transfer due to previous reproductive failure, but more field observations are required to test this hypothesis. Both adult and subadult female R. roxellana transfer from higherranking units to lower-ranking units: female dispersal is thus not related to the dominance hierarchy of resident males. Moreover, in each case, the resident male of the units from which females emigrated was still capable of breeding in the OMU; these cases therefore, do not support the hypothesis that females deserted the OMU because the resident males were at the end of their breeding tenures, and this is also what has been found in other colobine species (e.g., Procolobus verus: Korstjens and Schippers, 2003). The inbreeding avoidance hypothesis predicts natal dispersal in polygynous groups (Perrin and Mazalov, 1999). Inbreeding avoidance may induce dispersal of natal nulliparous females in species where fathers are still resident when their daughters mature (Lawson Handley and Perrin, 2007). For R. roxellana, male takeover, as one form of individual dispersal, has been found in only one case within our focal group over about 6 years (from winter 2001 to spring 2007) (Zhao et al., 2008b). Given the rarity of male takeover, inbreeding is theoretically a possibility, with the resident male copulating with his female offspring if they mature before the male tenure is over and have not yet emigrated, as has been noted in other langur species (e.g., Presbytis thomasi: Sterck et al., 2005). In such a condition, inbreeding avoidance could explain the subadult female dispersal (natal dispersal) that we have witnessed for the first time. In other words, inbreeding avoidance is the possible proximate factor driving subadult female dispersal in R. roxellana. Our findings help to create a picture of female dispersal in this species in the Qinling Mountains. Mate competition is the apparent driving force behind adult female dispersal, and inbreeding avoidance is the possible proximate factor promoting subadult female dispersal. Adult females show various reproductive strategies related to their dispersal activity so as to increase their reproductive success. This still leaves some questions, however, as to causes of the female dispersal patterns. For example, the influence of provisioning on female dispersal should be considered even though there is very limited provisioned food available, and only during a short period, it may indeed to some extent have affected female dispersal, and may have influenced our judgment as to whether resource competition serves as one proximate factor, although adult females were found to transfer into significantly smaller OMUs. Future investigations should be integrated with genetic methods so as to further evaluate how dispersal translates into gene flow in order to undertake appropriate measures for more efficient conservation of this species. Acknowledgments Permission to conduct this research was granted by the Zhouzhi National Nature Reserve. We strictly comply with the current laws of China in our research. The authors are indebted to Dr. Carola Borries (Stony Brook University, USA) for her constructive opin-
169
ions on the first draft of this paper. We would like to express our gratitude to the Editor Dr. Frank Cézilly, as well as Dr. Louise Barrett and one anonymous referee for their insightful comments on the manuscript. We appreciate Prof. Colin P. Groves (Australia National University) and Prof. Alan F. Dixson (Victoria University of Wellington) for their friendly help with English expression. We are grateful to Dr. Nicolas Perrin (University of Lausanne, Switzerland), for supplying a relevant reference. Dapeng Zhao expresses special thanks to Miss Yisha Ha for her sincere support. Thanks are extended to many local indigenous people who assisted us while doing long-term field work in the Zhouzhi National Nature Reserve. This research is funded by on-going grants from the Natural Science Foundation of China (Nos. 30770375; 30570312; 30630016), Cosmo Oil Eco Card Fund of Japan (2005–2010) and Northwest University Doctorate Dissertation of Excellence Funds (07YYB06). References Altmann, S., Altmann, J., 1977. On the analysis of rates of behavior. Anim. Behav. 25, 364–372. Altmann, S., Wagner, S., Levington, S., 1977. Two models for the evolution of polygyny. Behav. Ecol. Sociobiol. 2, 397–410. Borries, C., Larney, E., Derby, A.M., Koenig, A., 2004. Temporary absence and dispersal in Phayre’s leaf monkeys (Trachypithecus phayrei). Folia Primatol. 75, 27–30. Brockelman, W.Y., Reichard, U., Treesucon, U., Raemaekers, J.J., 1998. Dispersal, pair formation and social structure in gibbons. Behav. Ecol. Sociobiol. 42, 329–339. Chen, F.G., Min, Z.L., Lou, S.Y., Xie, W.Z., 1983. An observation on the behavior and some ecological habits of the Sichuan snub-nosed monkeys (Rhinopitheus roxellana) in Qinling Mountains. Acta Theriol. Sinica 3, 141–146. Clobert, J., Danchin, E., Dohndt, A.A., Nichols, J.D., 2001. Dispersal. Oxford University Press, Oxford. Davies, N.B., 1991. Mating systems. In: Krebs, J.R., Davies, N.B. (Eds.), Behavioural Ecology. Blackwell, Oxford, pp. 263–294. Dunbar, R.I.M., 1988. Primate Social Systems. Cornell University Press, New York. Greenwood, P.J., 1980. Mating systems, philopatry, and dispersal in birds and mammals. Anim. Behav. 28, 1140–1162. Haddow, A.J., 1952. Field and laboratory studies on an African monkey Cercopithecus ascanius schmidti Matschie. Proc. Zool. Soc. Lond. 122, 297–394. Harcourt, A.H., 1978. Strategies of emigration and transfer by primates, with particular reference to gorillas. Z. Tierpsychol. 48, 401–420. Isbell, L.A., van Vuren, D., 1996. Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour 133, 1–36. Janson, C.H., Goldsmith, M.L., 1995. Predicting group size in primates: foraging costs and predation risks. Behav. Ecol. Sociobiol. 6, 326–336. Jones, C.B., 1980. The functions of status in the mantled howler monkey Alouatta palliata GRAY: intra-specific competition for group membership in a folivorous Neotropical primate. Primates 21, 389–405. Kappeler, P.M., 1997. Intrasexual selection in Mirza coquereli: evidence for scramble competition polygyny in a solitary primate. Behav. Ecol. Sociobiol. 45, 115–127. Korstjens, A.H., Schippers, E.P., 2003. Dispersal patterns among Olive colobus in Tai national park. Int. J. Primatol. 24, 515–539. Lawson Handley, L.J., Perrin, N., 2007. Advances in our understanding of mammalian sex-biased dispersal. Mol. Ecol. 16, 1559–1578. Li, B.G., Zhao, D.P., 2007. Copulation behavior within one-male groups of wild Rhinopithecus roxellana in the Qinling Mountains of China. Primates 48, 190–196. Li, B.G., Li, H.Q., Zhao, D.P., Zhang, Y.H., 2006. Study on dominance hierarchy of Sichuan snub-nosed monkey (Rhinopithecus roxellana) in the Qinling Mountains. Acta Theriol. Sinica 26, 18–25. Marsh, C.W., 1979. Female transfer and mate choice among Tana River red colobus. Nature 281, 568–569. Martin, P., Bateson, P., 2007. Measuring Behaviour, third edition. Cambridge University Press, Cambridge. Monard, A.M., Duncan, P., 1996. Consequences of natal dispersal in female horses. Anim. Behav. 52, 565–579. Moore, J., 1984. Female transfer in primates. Int. J. Primatol. 5, 537–589. Möller, L.M., Beheregaray, L.B., 2004. Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus). Mol. Ecol. 13, 1607–1612. Murai, T., Mohamed, M., Bernard, H., Mahedi, P.A., Saburi, R., Higashi, S., 2007. Female transfer between one-male groups of proboscis monkey. Primates 48, 117–121. Paul, A., 2002. Sexual selection and mate choice. Int. J. Primatol. 23, 877–904. Perrin, N., Mazalov, V., 1999. Dispersal and inbreeding avoidance. Am. Nat. 154, 282–292. Petit, E., Balloux, F., Goudet, J., 2001. Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution 55, 635–640. Pusey, A.E., 1992. The primate perspective on dispersal. In: Stenseth, N.C., Lidicker Jr., W.Z. (Eds.), Animal Dispersal: Small Mammals as a Model. Chapman and Hall, London, pp. 243–259. Pusey, A.E., Packer, C., 1987. Dispersal and philopatry. In: Smuts, B.B., Cheney, D.L., Seyfarth, R.M., Wrangham, R.W., Struhsaker, T.T. (Eds.), Primate Societies. University of Chicago Press, Chicago, pp. 250–266.
170
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170
Reynolds, J., 1996. Animal breeding systems. Trends Ecol. Evol. 11, 68–72. Smuts, B.B., 1987. Sexual competition and mate choice. In: Smuts, B.B., Cheney, D.L., Seyfarth, R.M., Wrangham, R.W., Struhsaker, T.T. (Eds.), Primate Societies. University of Chicago Press, Chicago, pp. 385–399. Sterck, E.H.M., Willems, E.P., van Hooff, J.A.R.A.M., Wich, S.A., 2005. Female dispersal, inbreeding avoidance and mate choice in Thomas langurs (Presbytis thomasi). Behaviour 142, 845–868. Stokes, E.J., Parnell, R.J., Olejniczak, C., 2003. Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behav. Ecol. Sociobiol. 54, 329–339. Watts, D.P., 1990. Ecology of gorillas and its relation to female transfer in mountain gorillas. Int. J. Primatol. 11, 21–45. Yan, C.E., Jiang, Z.G., 2006. Does estradiol modulate sexual solicitations in female Rhinopithecus roxellana? Int. J. Primatol. 27, 1171–1186. Zhang, S.Y., Liang, B., Wang, L.X., 1999. Infanticide within captive groups of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Folia Primatol. 70, 274–276. Zhao, D.P., Gao, X., Li, B.G., Watanabe, K., 2008a. First wild evidence of neonate nipple preference and maternal cradling laterality in Old World monkeys:
a preliminary study from Rhinopithecus roxellana. Behav. Process. 77, 364– 368. Zhao, D.P., Li, B.G., Groves, C.P., Watanabe, K., 2008b. Impact of male takeover on intra-unit sexual interactions and subsequent interbirth interval in wild Rhinopithecus roxellana. Folia Primatol. 79, 93–102. Zhao, D.P., Ji, W.H., Watanabe, K., Li, B.G., 2008c. Hand preference of unimanual and bimanual reaching actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Am. J. Primatol. 70, 500–504. Zhao, D.P., Li, B.G., Watanabe, K., 2008d. First evidence on foot preference during locomotion in Old World monkeys: a study of quadrupedal and bipedal actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Primates, doi:10.1007/s10329-008-0096-z. Zhao, D.P., Li, B.G., Li, Y.H., Wada, K., 2005. Extra-unit sexual behavior among wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Folia Primatol. 76, 172–176. Zumpe, D., Michael, R.P., 1986. Dominance index: a simple measure of relative dominance status in primates. Am. J. Primatol. 10, 291–301.
Contents lists available at ScienceDirect
Behavioural Processes journal homepage: www.elsevier.com/locate/behavproc
Mate competition and reproductive correlates of female dispersal in a polygynous primate species (Rhinopithecus roxellana) Dapeng Zhao a , Weihong Ji b , Baoguo Li a,∗ , Kunio Watanabe c a
College of Life Sciences, Northwest University, Xi’an, China Institute of Natural Resources, Massey University, Auckland, New Zealand c Primate Research Institute, Kyoto University, Inuyama, Aichi, Japan b
a r t i c l e
i n f o
Article history: Received 27 March 2008 Received in revised form 9 July 2008 Accepted 13 July 2008 Keywords: Female dispersal Mate competition Polygynous Reproductive output Sichuan snub-nosed monkeys
a b s t r a c t Different mating systems in group-living animals have characteristic behavioral correlates that are primarily related to mate competition. Mate competition may push individuals to selectively make dispersal decisions for the purpose of maximizing of opportunities for reproduction. The Sichuan snub-nosed monkey (Rhinopithecus roxellana) is a polygynous primate species endemic to China. We provide the first data on female dispersal in a free-ranging group of R. roxellana in the Zhouzhi National Nature Reserve, Qinling Mountains, China. Both adult and subadult female dispersal occurred. Immigration/emigration rates of adult females are higher than those of subadult females. Mate competition is one apparent driving force behind adult female dispersal, and inbreeding avoidance is the possible proximate factor influencing subadult female dispersal. Adult female R. roxellana employ various reproductive strategies related to dispersal, which may increase their reproductive success. © 2008 Elsevier B.V. All rights reserved.
1. Introduction Groups of many animal species contain adults of both sexes. Based on current socioecological theory, the mating system of a species or population is determined by the spatial and temporal distribution of adult males and receptive females, i.e. their social organization (Davies, 1991; Reynolds, 1996). Different mating systems, especially in primate species, have characteristic behavioral correlates that are primarily related to mate competition in the same sex (e.g., Kappeler, 1997). For instance, mate competition may push individuals to selectively transfer between groups for the purpose of maximization of their reproduction (e.g., Cetacea: Tursiops aduncus, Möller and Beheregaray, 2004; Chiroptera: Nyctalus noctula, Petit et al., 2001; Perissodactyla: Equus caballus, Monard and Duncan, 1996; Primates: Hylobates lar, Brockelman et al., 1998). Primate societies are characterized by high rates of dispersal of individuals (Greenwood, 1980; Pusey, 1992). In a large number of primate species, males tend to disperse more than females; in other species, however, both sexes disperse, or dispersal is femalebiased (Pusey and Packer, 1987; Isbell and van Vuren, 1996). The proximate causes of primate dispersal, which obviously differ in
∗ Corresponding author at: College of Life Sciences, Northwest University, North TaibaiRoad No. 229, Xi’an, Shaanxi Province 710069, China. Tel.: +86 29 88302048; fax: +86 29 88303572. E-mail addresses: [email protected] (D. Zhao), [email protected] (B. Li). 0376-6357/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2008.07.006
different species and among individuals of different age/sex classes within the same species, may include mate competition, mate choice, resource competition and inbreeding avoidance (Clobert et al., 2001; Lawson Handley and Perrin, 2007). For Old World monkey species, male-biased dispersal has been well documented, as have certain notable exceptions, including hamadryas baboons, red colobus and black colobus (Pusey and Packer, 1987): female transfers are very rare in Old World monkeys (Moore, 1984), but do occur in some langur species (Procolobus badius: Marsh, 1979; Trachypithecus phayrei: Borries et al., 2004; Presbytis thomasi: Sterck et al., 2005). Darwin’s theory of sexual selection is expressed, within groups, both in direct competition between members of the same sex and in the mating preferences of one sex for the other (Paul, 2002). In primate research, female mate competition over males is especially important in polygynous species, although male–male competition for mates and female mate choice are both common (Smuts, 1987). The Sichuan snub-nosed monkey (Rhinopithecus roxellana), a strict seasonal breeder, is a polygynous colobine species; its basic social and reproductive unit is the one-male unit (OMU), which consists of a single resident male, a number of adult females, subadult females, juveniles and infants (Chen et al., 1983; Li and Zhao, 2007). It has been suggested that sexual competition in this polygynous species may have a skewed representation: females faced with multiple competitors will exhibit a high level of sexual competition, i.e. female mate competition, while the single resident male will not experience within-unit sexual competition.
166
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170
Female R. roxellana strives for greater copulation access to the sole resident male by behavioral strategies such as sexual interference (Li and Zhao, 2007). To date, research on individual dispersal in R. roxellana is still in its infancy, and so far has focused on male dispersal, which generally occurs when an OMU’s young males reach about 4 years of age or when the adult male is replaced by another male from an all-male group (Chen et al., 1983). No systematic reports have been published on female dispersal or factors influencing it. Here, we present the first data on female dispersal and individual reproductive output in a free-ranging group of R. roxellana where all members are individually recognized according to their physical characteristics. Data are from long-term records accumulated at Zhouzhi National Nature Reserve in the Qinling Mountains, China. The main purpose of this paper is to investigate whether both adult female dispersal (breeding dispersal) and subadult female dispersal (natal dispersal) occur in this species, to explore whether mate competition drives female dispersal, and to discuss female reproductive strategies behind this behavior. 2. Methods
(a) Adult female: No less than 5 years, about half the body size of adult males. The golden guard hairs in the cape area were much shorter than those of adult males. Their breasts and nipples were large and easily seen. (b) Subadult female: Three to four years old, about two-thirds the body size of adult females. They lacked golden guard hairs in the cape and their breasts and nipples were significantly smaller than those of adult females. (c) Infant: Zero months to one year old. Their hair is light brownish gray or light brown, appearing white in sunshine. They are sometimes observed playing with juveniles or other infants, but spend most of their time beside their mothers or sucking milk from adult females. 2.4. Measuring female dispersal In gregarious primates, dispersal refers to a change in group membership (Pusey and Packer, 1987). We also define dispersal as leaving or entering the OMU within the focus group, not necessarily accompanied by a change in range. When dispersal involves a female emigrating from one OMU and immigrating to another OMU within the focal group, we refer to it as female transfer.
2.1. Study site and species 2.5. Data collection This study was carried out in the Zhouzhi National Nature Reserve, which was established in 1985 to protect 52,931 km2 of temperate forest on the northern slopes of the Qinling Mountains, China (Li and Zhao, 2007; Zhao et al., 2008a,b,c,d). The study animals were members of one R. roxellana group, consisting of OMUs that travel together all the day. The focal group, as one open population, is unstable as several OMUs disappeared from or appeared in it; the group size ranged from 61 to 116 individuals during the observation period. 2.2. Food provisioning In October 2001 we began to habituate the focal group. A 15 m × 30 m provisioning site was set up at Sanchakou (1646 m above sea level) in Gongnigou valley (33◦ 48 68 N, 108◦ 16 18 E). The assistants searched for monkeys of the focal group and attracted them to the provisioning site at approximately 9:00 every day when research was being conducted. Artificial factors, such as leading monkeys to the provisioning site by assistants, especially in the early periods, might have influenced the monkeys’ behavior and social activities, but they soon habituated to the provisioning site, so reducing outside influence (Zhao et al., 2008a,b,c,d). Apples, radishes, and corn were provided three times per day, approximately 200 g per monkey per day in total. Compared with the daily total diet of R. roxellana, energy intake from the provisioned food is very limited and thus its influence would on the whole be minimal (Li and Zhao, 2007). After successful habituation, the group could be observed daily. At night, the monkeys’ roosts were ordinarily located within a 3 km radius of the provisioning site. At the end of the observation period, the monkeys were free-living in the region of the west ridge. During the study period we obtained behavioral data from distances between 0.5 and 50 m. 2.3. Individual identification and age class By late November 2001, all members were individually recognized by prominent physical characteristics, such as body size, pelage color, hair patterns, or physical disabilities (Zhao et al., 2005, 2008a,b,c,d). In this study, we focus on two age classes of female monkeys and the infant class, which are defined as follows:
Observations were made from October 2001 to May 2005 (316 observation days, 1736.2 observation hours in total). We recorded changes in group composition and checked the animals during each observation month, especially the first observation week during each study period. For female dispersal events the group of origin and destination were noted if possible, as well as whether the female concerned was subadult or adult, and whether the female was caring or not caring for an infant. The mating season, from late September to early December, and the birth season, from March to May, respectively, were defined according to Li and Zhao (2007). Birth data on the focal group were gathered during each birth season from 2002 to 2006, as described by Zhao et al. (2008b). Furthermore, we recorded agonistic encounters between resident males of different OMUs via the “all occurrences” and “behavioral sampling” methods (Martin and Bateson, 2007). Description of the forms of aggression and submission followed Li et al. (2006). 2.6. Data analysis Unit size refers to weaned individuals only (Table 1). Dependent offspring are not considered to represent effective feeding competitors (Janson and Goldsmith, 1995), based on models in Dunbar (1988), and are generally excluded from the analysis and discussion. Birth rates were measured as actual births/female/year for OMUs of different sizes and for different numbers of females per OMU. Calculation methods were based upon the description by Watts (1990). Within the social structure of R. roxellana, the rank of the OMU is represented by its resident male’s rank (Li et al., 2006). For the dominance of resident males in the focal group, we calculated a dominance index (Zumpe and Michael, 1986). This index, expressed as a percentage, is based on the number and direction of aggressive and submissive behaviors exchanged among resident males, as described in detail by Li et al. (2006). In this paper, changes in size and composition of groups were similarly treated as independent data points, following Stokes et al. (2003). Different subsets of the same individuals were commonly treated as independent groups (Altmann and Altmann, 1977). Statistical analyses were conducted in SPSS 12.0. All tests were two-tailed and the results were considered significant at p < 0.05.
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170 Table 1 OMU size and composition of Polygynous Rhinopithecus roxellana Unit ID
Unit composition TOT-I
TOT + I
M/SAF
AF/SAF
BaZiTou ChangMao DuanZhi FangPian HongDian HeiTou JingZiTou LuoPan PengKe TuTou ZhongZhi
9.63 9.86 7.90 7.50 11.86 7.75 8.38 15.4 5.00 7.75 5.00
11.50 11.14 9.40 7.50 14.43 8.63 11.38 20.00 5.75 9.75 5.50
M/AF 0.25 0.30 0.24 0.50 0.19 0.31 0.23 0.14 0.33 0.22 0.50
0.50 0.50 1.67 1.00 0.50 0.88 0.72 0.42 1.00 2.00 0.50
2.00 1.64 7.00 2.00 2.57 2.89 3.18 3.00 3.00 9.00 1.00
n AF 4.00 3.28 4.20 2.00 5.14 3.25 4.38 7.20 3.00 4.50 2.00
n SAF 2.00 2.00 0.60 1.00 2.00 1.13 1.38 2.40 1.00 0.50 2.00
Mean ±S.D.
8.73 ±2.97
10.45 ±4.12
0.29 ±0.12
0.88 ±0.52
3.84 ±2.59
3.92 ±1.48
1.33 ±0.67
Note: For those units within the focal group we use one count per observation month and then calculated the median. TOT-I = the whole group size excluding infants; TOT + I = the whole group size including infants; M/AF = the resident male–adult females ratio; M/SAF = the resident male–subadult females ratio; AF/SAF = adult females–subadult females ratio; n AF = numbers of adult females in the unit; n SAF = numbers of subadult females in the unit.
3. Results A total of 20 immigration and 17 emigration events (Fig. 1) was recorded involving 21 adult females (80.77%) and 5 subadult females (19.23%). It includes 11 transfers between known units, i.e. inter-unit female transfer (8 adult females, 72.73% and 3 subadult females, 27.27%), with the remainder consisting of 6 emigrations
167
from and 9 immigrations into the focal group. 17 adult females and 3 subadult females immigrated (1 immigration every 0.21 adult female years, 1 immigration every 0.83 subadult female years). 12 adult females and 5 subadult females emigrated (1 emigration every 0.30 adult female years, 1 emigration every 0.72 subadult female years). We found that there was no female who dispersed more than once in this study. All adult female transfers occurred in the interval between the birth season and mating season (birth season–mating season interval (June to early September): 51.74%; mating season–birth season interval (middle December to February): 48.26%). Subadult female transfers mainly took place in the interval between the mating season and birth season and also occurred in the early mating season (birth season–mating season interval: 50.00%; mating season–birth season interval: 25.00%; early mating season: 25.00%). 3.1. Dispersal in relation to unit size and intra-unit female number For 11 cases of female transfer between known OMUs of the focal group, adult females were found to transfer into significantly smaller OMUs (Wilcoxon signed ranks test: n = 8, Z = −2.565, p = 0.010). This finding did not apply to subadult females (n = 3, Z = −1.604, p = 0.109). Neither adult females nor subadult females showed significant preferences for OMUs with fewer females (i.e. including adult plus subadult individuals (Wilcoxon signed ranks test: adult females, n = 8, Z = −1.890, p = 0.059 and subadult females, n = 3, Z = −1.342, p = 0.180)). Adult females, however, showed significant preference for OMUs containing fewer adult females (Wilcoxon signed ranks test: n = 8, Z = −2.598, p = 0.009) while
Fig. 1. Female transfer in the focal group. Solid lines indicate all females present were counted. Dotted lines indicate not all female were counted in the focal group. Arrows indicate transfers in and out of the group. A means “adult female”, S means “subadult female”, MT means “male takeover occurred”, MD means “resident male disappeared”, MJ means “a new male joined”. Superscripts: a means “the adult female transfer when she is pregnant”, b means “the adult female transfer with her new infant”, and c means means “the one-male unit joined the focal group”, means “the one-male unit disappeared during the “the adult female transfer after her infant disappeared”; means “the disappearance of the one-male unit was noted after an interruption of observations”. observation”,
168
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170
subadult females did not (n = 3, Z = −1.000, p = 0.317). In addition, subadult females showed no preference for OMUs with fewer subadult females (n = 3, Z = −0.535, p = 0.593). For 15 cases of female dispersal consisting of 6 emigrations out of and 9 immigrations into the focal group, the OMU from which an adult female emigrated, or into which an adult female immigrated, did not differ in mean unit size from the focal group (one-sample ttest: emigration, d.f. = 3, t = −0.676, p = 0.548; immigration, d.f. = 8, t = 0.799, p = 0.447). Similarly, the size of the OMU from which a subadult female emigrated did not differ from the mean size of OMUs within the focal group (d.f. = 1, t = −0.820, p = 0.563). Adult females left or joined an OMU with both a similar total of females (one-sample t-test: emigration, d.f. = 3, t = 0.001, p = 1.000; immigration, d.f. = 8, t = 1.107, p = 0.301) and a similar number of adult females (one-sample t-test: emigration, d.f. = 3, t = 1.320, p = 0.279; immigration, d.f. = 8, t = 1.620, p = 0.144) compared with mean numbers among OMUs in the focal group. Similarly, subadult females emigrate from an OMU with both a similar total of females (one-sample t-test: d.f. = 1, t = 0.750, p = 0.590) and similar total of subadult females (d.f. = 1, t = 0.670, p = 0.624) compared with mean numbers among OMUs in the focal group. 3.2. Dispersal in relation to female reproductive status Female Sichuan snub-nosed monkeys generally give birth every second year (Zhao et al., 2008b). During our study, adult female dispersal could be simply divided into four different categories according to reproductive status: (1) Pregnant females’ transfer: During the mating season–birth season interval, three females (JinGu, LiuLiu, and TieMao) transferred when they were likely to be pregnant (Yan and Jiang, 2006). (2) Lactating females’ transfer: Three adult females (PianFen, BaiXian, and WeiZhiMing) transferred with their newborn infants. The infants survived in their new units. WeiZhiMing gave birth in the first post-immigration birth season while PianFen and BaiXian gave birth in the second post-immigration birth season. (3) One adult female, HeiDian, made an inter-unit transfer after her newborn infant disappeared for unknown reasons. She gave birth in both the following two post-immigration birth seasons. (4) For the remaining other 14 adult females, 6 who moved during the birth season–mating season interval gave birth in the following 2 post-immigration birth seasons (83.33% in the first birth season and 16.67% in the second birth season). There were no births recorded for any of the eight females who immigrated in the mating season–birth season interval during the following two post-immigration birth seasons. All infants born to immigrating females survived. Most of the adult females that emigrated had not given birth during the preceding birth season. Overall, 76.47% of adult females and 66.67% of subadult females experience reproductive success within two post-immigration birth seasons. Birth rate is significantly correlated to both unit size and unit female numbers (Pearson correlation test: unit size, rs = 0.687, p < 0.001; unit female numbers, rs = 0.710, p < 0.001). Conversely, infant survivorship is not significantly correlated with either group size or female group size (Pearson correlation test: unit size, rs = 0.094, p = 0.634; unit female numbers, rs = −0.033, p = 0.866). 3.3. Dispersal in relation to OMU rank In all cases females (adults and subadults) transferred from higher-ranking to lower-ranking OMUs. In all cases the OMUs from
which females emigrated contained a resident male that was sexually active and capable of siring offspring, given the birth data. The phenomenon of male takeover, a form of individual dispersal, has been found in only one case within the focal group. The intruding male, JiaBan, superseded the resident male, HeiTou, and became the new resident male, after which the old resident male, HeiTou, left the focal group on April 28th 2003. During our study period, no female dispersal occurred in this OMU whereas female dispersal prevailed in other OMUs where no male takeover occurred. 4. Discussion To our knowledge, this is the first report of female dispersal in any species of Rhinopithecus. Both adult and subadult female R. roxellana are involved in dispersal activity. Immigration rates and emigration rates of adult females are higher than those of subadult females, which contrasts with the findings of some other colobine studies, such as Nasalis larvatus (Murai et al., 2007). In previous research, it was believed that only male dispersal occurs in R. roxellana (Chen et al., 1983). We report, for the first time, that R. roxellana displays dispersal of both sexes, as in some other colobine species (e.g., Procolobus verus: Korstjens and Schippers, 2003), although to date it could not be identified whether there is female-biased dispersal or male-biased dispersal in this species. The mate competition hypothesis explains dispersal by the sex that competes most over access to reproductive partners (Clobert et al., 2001). As regards inter-unit transfers, adult female R. roxellana tend to transfer into those OMUs with few adult females, which suggests that female mate competition should be involved. Of the major explanations for female dispersal, another that is widely applicable to polygynous primates is the “competitive female choice” model (Altmann et al., 1977), which holds that females are choosing to transfer in order to maximize their reproductive success. For R. roxellana in this study, 76.47% of adult females and 66.67% of subadult females show reproductive success within two post-immigration birth seasons, compared to a low birth rate in the original unit during the birth season preceding immigration. This suggests that females transfer between OMUs because doing so may increase their reproductive success; to some extent supporting the “competitive female choice” model (Altmann et al., 1977). In theory, however, the lactating females that made interunit transfers would be expected to be vulnerable to infanticide, which has been reported in this species under captive conditions (Zhang et al., 1999); this is a question which must be left for future consideration. The timing of dispersal could provide interesting clues to ultimate causes (Lawson Handley and Perrin, 2007). “Extra-group attraction” has been shown to drive emigration in several groupliving primate species such as chimpanzees, macaques, mangabeys, vervets and guenons (Lawson Handley and Perrin, 2007). In this case, the timing of dispersal generally coincides with the mating season. Adult female dispersal in R. roxellana did not take place in the mating season but in the interval between the birth season and the mating season, and adult females who shifted in the birth season–mating season interval gave birth in the following two post-immigration birth seasons. This suggests that the choice of the dispersal period in female R. roxellana is crucial for subsequent reproductive success although extra-group attraction may not be the driving factor for female dispersal in this species. Zhao et al. (2008b) reported that after the male takeover, the new resident male made use of the birth season-mating season interval to establish reproductive relationships. It may thus be inferred that adult females which choose the birth season–mating season interval to disperse may be adopting a similar reproductive strategy.
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170
Though it is hard to confirm, there is an intriguing suggestion that pregnant females emigrate/transfer at a higher than expected rate in some female transfer species (e.g., Cercopithecus ascanius: Haddow, 1952; Alouatta palliata: Jones, 1980). Three such cases were observed in female R. roxellana, where pregnant females chose the mating season–birth season interval to transfer into smaller units. This suggests that pregnant females may avoid feeding competition within the resident unit and ensure that their coming offspring will have better food resources in a new unit. In addition, some female transfers in primates (e.g., gorillas and chacma baboons) followed reproductive failure, i.e. death of the infant (Harcourt, 1978). In this study, one similar event occurred. It is possible that female R. roxellana may transfer due to previous reproductive failure, but more field observations are required to test this hypothesis. Both adult and subadult female R. roxellana transfer from higherranking units to lower-ranking units: female dispersal is thus not related to the dominance hierarchy of resident males. Moreover, in each case, the resident male of the units from which females emigrated was still capable of breeding in the OMU; these cases therefore, do not support the hypothesis that females deserted the OMU because the resident males were at the end of their breeding tenures, and this is also what has been found in other colobine species (e.g., Procolobus verus: Korstjens and Schippers, 2003). The inbreeding avoidance hypothesis predicts natal dispersal in polygynous groups (Perrin and Mazalov, 1999). Inbreeding avoidance may induce dispersal of natal nulliparous females in species where fathers are still resident when their daughters mature (Lawson Handley and Perrin, 2007). For R. roxellana, male takeover, as one form of individual dispersal, has been found in only one case within our focal group over about 6 years (from winter 2001 to spring 2007) (Zhao et al., 2008b). Given the rarity of male takeover, inbreeding is theoretically a possibility, with the resident male copulating with his female offspring if they mature before the male tenure is over and have not yet emigrated, as has been noted in other langur species (e.g., Presbytis thomasi: Sterck et al., 2005). In such a condition, inbreeding avoidance could explain the subadult female dispersal (natal dispersal) that we have witnessed for the first time. In other words, inbreeding avoidance is the possible proximate factor driving subadult female dispersal in R. roxellana. Our findings help to create a picture of female dispersal in this species in the Qinling Mountains. Mate competition is the apparent driving force behind adult female dispersal, and inbreeding avoidance is the possible proximate factor promoting subadult female dispersal. Adult females show various reproductive strategies related to their dispersal activity so as to increase their reproductive success. This still leaves some questions, however, as to causes of the female dispersal patterns. For example, the influence of provisioning on female dispersal should be considered even though there is very limited provisioned food available, and only during a short period, it may indeed to some extent have affected female dispersal, and may have influenced our judgment as to whether resource competition serves as one proximate factor, although adult females were found to transfer into significantly smaller OMUs. Future investigations should be integrated with genetic methods so as to further evaluate how dispersal translates into gene flow in order to undertake appropriate measures for more efficient conservation of this species. Acknowledgments Permission to conduct this research was granted by the Zhouzhi National Nature Reserve. We strictly comply with the current laws of China in our research. The authors are indebted to Dr. Carola Borries (Stony Brook University, USA) for her constructive opin-
169
ions on the first draft of this paper. We would like to express our gratitude to the Editor Dr. Frank Cézilly, as well as Dr. Louise Barrett and one anonymous referee for their insightful comments on the manuscript. We appreciate Prof. Colin P. Groves (Australia National University) and Prof. Alan F. Dixson (Victoria University of Wellington) for their friendly help with English expression. We are grateful to Dr. Nicolas Perrin (University of Lausanne, Switzerland), for supplying a relevant reference. Dapeng Zhao expresses special thanks to Miss Yisha Ha for her sincere support. Thanks are extended to many local indigenous people who assisted us while doing long-term field work in the Zhouzhi National Nature Reserve. This research is funded by on-going grants from the Natural Science Foundation of China (Nos. 30770375; 30570312; 30630016), Cosmo Oil Eco Card Fund of Japan (2005–2010) and Northwest University Doctorate Dissertation of Excellence Funds (07YYB06). References Altmann, S., Altmann, J., 1977. On the analysis of rates of behavior. Anim. Behav. 25, 364–372. Altmann, S., Wagner, S., Levington, S., 1977. Two models for the evolution of polygyny. Behav. Ecol. Sociobiol. 2, 397–410. Borries, C., Larney, E., Derby, A.M., Koenig, A., 2004. Temporary absence and dispersal in Phayre’s leaf monkeys (Trachypithecus phayrei). Folia Primatol. 75, 27–30. Brockelman, W.Y., Reichard, U., Treesucon, U., Raemaekers, J.J., 1998. Dispersal, pair formation and social structure in gibbons. Behav. Ecol. Sociobiol. 42, 329–339. Chen, F.G., Min, Z.L., Lou, S.Y., Xie, W.Z., 1983. An observation on the behavior and some ecological habits of the Sichuan snub-nosed monkeys (Rhinopitheus roxellana) in Qinling Mountains. Acta Theriol. Sinica 3, 141–146. Clobert, J., Danchin, E., Dohndt, A.A., Nichols, J.D., 2001. Dispersal. Oxford University Press, Oxford. Davies, N.B., 1991. Mating systems. In: Krebs, J.R., Davies, N.B. (Eds.), Behavioural Ecology. Blackwell, Oxford, pp. 263–294. Dunbar, R.I.M., 1988. Primate Social Systems. Cornell University Press, New York. Greenwood, P.J., 1980. Mating systems, philopatry, and dispersal in birds and mammals. Anim. Behav. 28, 1140–1162. Haddow, A.J., 1952. Field and laboratory studies on an African monkey Cercopithecus ascanius schmidti Matschie. Proc. Zool. Soc. Lond. 122, 297–394. Harcourt, A.H., 1978. Strategies of emigration and transfer by primates, with particular reference to gorillas. Z. Tierpsychol. 48, 401–420. Isbell, L.A., van Vuren, D., 1996. Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour 133, 1–36. Janson, C.H., Goldsmith, M.L., 1995. Predicting group size in primates: foraging costs and predation risks. Behav. Ecol. Sociobiol. 6, 326–336. Jones, C.B., 1980. The functions of status in the mantled howler monkey Alouatta palliata GRAY: intra-specific competition for group membership in a folivorous Neotropical primate. Primates 21, 389–405. Kappeler, P.M., 1997. Intrasexual selection in Mirza coquereli: evidence for scramble competition polygyny in a solitary primate. Behav. Ecol. Sociobiol. 45, 115–127. Korstjens, A.H., Schippers, E.P., 2003. Dispersal patterns among Olive colobus in Tai national park. Int. J. Primatol. 24, 515–539. Lawson Handley, L.J., Perrin, N., 2007. Advances in our understanding of mammalian sex-biased dispersal. Mol. Ecol. 16, 1559–1578. Li, B.G., Zhao, D.P., 2007. Copulation behavior within one-male groups of wild Rhinopithecus roxellana in the Qinling Mountains of China. Primates 48, 190–196. Li, B.G., Li, H.Q., Zhao, D.P., Zhang, Y.H., 2006. Study on dominance hierarchy of Sichuan snub-nosed monkey (Rhinopithecus roxellana) in the Qinling Mountains. Acta Theriol. Sinica 26, 18–25. Marsh, C.W., 1979. Female transfer and mate choice among Tana River red colobus. Nature 281, 568–569. Martin, P., Bateson, P., 2007. Measuring Behaviour, third edition. Cambridge University Press, Cambridge. Monard, A.M., Duncan, P., 1996. Consequences of natal dispersal in female horses. Anim. Behav. 52, 565–579. Moore, J., 1984. Female transfer in primates. Int. J. Primatol. 5, 537–589. Möller, L.M., Beheregaray, L.B., 2004. Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus). Mol. Ecol. 13, 1607–1612. Murai, T., Mohamed, M., Bernard, H., Mahedi, P.A., Saburi, R., Higashi, S., 2007. Female transfer between one-male groups of proboscis monkey. Primates 48, 117–121. Paul, A., 2002. Sexual selection and mate choice. Int. J. Primatol. 23, 877–904. Perrin, N., Mazalov, V., 1999. Dispersal and inbreeding avoidance. Am. Nat. 154, 282–292. Petit, E., Balloux, F., Goudet, J., 2001. Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution 55, 635–640. Pusey, A.E., 1992. The primate perspective on dispersal. In: Stenseth, N.C., Lidicker Jr., W.Z. (Eds.), Animal Dispersal: Small Mammals as a Model. Chapman and Hall, London, pp. 243–259. Pusey, A.E., Packer, C., 1987. Dispersal and philopatry. In: Smuts, B.B., Cheney, D.L., Seyfarth, R.M., Wrangham, R.W., Struhsaker, T.T. (Eds.), Primate Societies. University of Chicago Press, Chicago, pp. 250–266.
170
D. Zhao et al. / Behavioural Processes 79 (2008) 165–170
Reynolds, J., 1996. Animal breeding systems. Trends Ecol. Evol. 11, 68–72. Smuts, B.B., 1987. Sexual competition and mate choice. In: Smuts, B.B., Cheney, D.L., Seyfarth, R.M., Wrangham, R.W., Struhsaker, T.T. (Eds.), Primate Societies. University of Chicago Press, Chicago, pp. 385–399. Sterck, E.H.M., Willems, E.P., van Hooff, J.A.R.A.M., Wich, S.A., 2005. Female dispersal, inbreeding avoidance and mate choice in Thomas langurs (Presbytis thomasi). Behaviour 142, 845–868. Stokes, E.J., Parnell, R.J., Olejniczak, C., 2003. Female dispersal and reproductive success in wild western lowland gorillas (Gorilla gorilla gorilla). Behav. Ecol. Sociobiol. 54, 329–339. Watts, D.P., 1990. Ecology of gorillas and its relation to female transfer in mountain gorillas. Int. J. Primatol. 11, 21–45. Yan, C.E., Jiang, Z.G., 2006. Does estradiol modulate sexual solicitations in female Rhinopithecus roxellana? Int. J. Primatol. 27, 1171–1186. Zhang, S.Y., Liang, B., Wang, L.X., 1999. Infanticide within captive groups of Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Folia Primatol. 70, 274–276. Zhao, D.P., Gao, X., Li, B.G., Watanabe, K., 2008a. First wild evidence of neonate nipple preference and maternal cradling laterality in Old World monkeys:
a preliminary study from Rhinopithecus roxellana. Behav. Process. 77, 364– 368. Zhao, D.P., Li, B.G., Groves, C.P., Watanabe, K., 2008b. Impact of male takeover on intra-unit sexual interactions and subsequent interbirth interval in wild Rhinopithecus roxellana. Folia Primatol. 79, 93–102. Zhao, D.P., Ji, W.H., Watanabe, K., Li, B.G., 2008c. Hand preference of unimanual and bimanual reaching actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Am. J. Primatol. 70, 500–504. Zhao, D.P., Li, B.G., Watanabe, K., 2008d. First evidence on foot preference during locomotion in Old World monkeys: a study of quadrupedal and bipedal actions in Sichuan snub-nosed monkeys (Rhinopithecus roxellana). Primates, doi:10.1007/s10329-008-0096-z. Zhao, D.P., Li, B.G., Li, Y.H., Wada, K., 2005. Extra-unit sexual behavior among wild Sichuan snub-nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains of China. Folia Primatol. 76, 172–176. Zumpe, D., Michael, R.P., 1986. Dominance index: a simple measure of relative dominance status in primates. Am. J. Primatol. 10, 291–301.