云南无量山印支灰叶猴社会结构初步研究

乌叶猴属物种主要以一雄多雌的小群活动,其群体大小一般不超过20只。泰国东北部的印支灰叶猴生活在一雄多雌或多雄多雌群的小群中,而云南无量山的印支灰叶猴却生活在多雄多雌的大群中,有些群大小超过100只,但是对无量山印支灰叶猴的社会结构缺乏研究。2012年9月至2015年7月,在云南无量山国家级自然保护区大寨子片区开展一群习惯化印支灰叶猴的社会结构研究。采用10min间隔的焦点动物瞬时记录法,记录焦点成年雄性5 m范围内不同性别年龄个体的数量。观察期间共有594次准确识别焦点雄性5 m范围内其它个体年龄性别的有效数据 (至少有1只其他个体)。其中,焦点雄性周围出现其它成年雄性的几率为44.2%,数量为(0.62 ± 0.85)只;同时出现成年雄性和成年雌性的几率是32.5%。取食时焦点雄性周围出现其它雄性的比例 (60.0%) 和数量 (平均0.93只) 都大于休息和移动时,数量最多为5只成年雄性。结果表明该群灰叶猴的社会结构不是由多个OMU和AMU组成的重层社会,而是多雄多雌的社会结构。无量山印支灰叶猴群内成年雄性间相互容忍度较高,个体的空间分布在取食时尤其密集,说明无量山印支灰叶猴的食物丰富 (至少在某些季节),这也部分解释了为什么无量山印支灰叶猴能够生活在大群中。本文为进一步研究亚洲疣猴社会结构的多样性和进化提供了重要的基础资料。     

Cultural transmission of snake-mobbing in free-ranging Hanuman langurs

A focal troop of free-ranging Hanuman langurs (Presbytis entellus) living in an open scrub forest around Jodhpur was observed mobbing poisonous snakes on two different occasions during field observations of about 4,109 h. These observations of snake-mobbing demonstrate that langurs exhibit a special behaviour against 'potentially dangerous animals' which is similar to the mobbing displays of birds, and of other primates. It is suggested that the adaptive significance of snake-mobbing among langurs lies in the 'cultural transmission' of this information. These observations further support the 'kin-selection' model.     

Female dispersal,social organization,and infanticide in langurs: Are they linked to human disturbance?

Female dispersal in gregarious animals can involve the desertion of a site, desertion of a social group, or both. Group desertion may be related to inbreeding avoidance. Group fidelity may result from cooperation among females in a group. Site fidelity will be more likely when food can be monopolized and when the population density is close to habitat saturation. The degree of habitat saturation was approximated with a measure of human disturbance. The influence of these various factors on the incidence of female dispersal was investigated for langur populations using data from the literature. The results suggest that female dispersal in langurs involved site desertion, not group desertion. The incidence of female dispersal may affect the social organization of langurs. I propose that when females do not disperse, male takeovers prevail, whereas in populations where female dispersal regularly occurs bisexual groups are disbanded or new groups are formed, a process I call female split-merger. Male takeover is thought to occur when site fidelity is high, female split-merger when site fidelity is low. These processes were indeed found to occur in these circumstances. The dispersal of females might prevent infanticide, whereas male takeover might promote it. Indeed, in studies with male takeover, more infants fell victim to infanticide than in studies with female split-merger. Therefore, female dispersal in langurs is an effective female counterstrategy to infanticide. The factor that had the most profound effect on female dispersal, social organization, and infanticide was habitat saturation. Habitat saturation was measured as the degree of human disturbance, and its influence on the behavior of langurs is probably of relatively recent date. This may lead to an evolutionary transient situation and may explain the discrepancy between current socioecological theories and the behavior of langurs in populations lacking female dispersal. Am. J. Primatol. 44:235–254, 1998. © 1998 Wiley-Liss, Inc.     

My primate studies

In this paper, I describe my 62 years in primatology focusing on some of the key findings from fieldwork conducted in Japan, India, and Africa. My first study on nonhuman primates described in detail the division of a troop of Japanese macaques at Takasakiyama. After that, I had an opportunity to work on Hanuman langurs at Dharwar, India. These langurs lived in one-male, multi-female groups. This type of group structure was maintained through takeovers by all-male parties. The adult male and all juvenile males were chased out of the group. By this process, the one-male, multi-female group system was maintained. The incoming adult male bit and killed all infants in the group. Mothers who lost their infants went into estrus and mated with the newly arrived male. For many years, scientists ignored these events or ruled them out as abnormal behavior. My work on Japanese macaques suggested that concentrated resources created by artificial feeding exaggerated dominance rank hierarchies among individuals, whereas it is comparatively relaxed in the natural environment. I also investigated the population dynamics of a troop and the life histories of individuals. From these studies, I documented the frequency of twin births, the carrying of dead infants by mothers, and the occurrence of physical malformations. These observations were made possible through artificial feeding, revealing the merits and demerits of this approach. I pointed out that authors and journal editors must be careful to acknowledge important elements of the environment where studies are conducted, and these should be described when reporting results in scientific articles. My studies of chimpanzees were conducted at Bossou, Guinea. I suggested that there are males who lived outside of bisexual groups. Chimpanzees in this population made and used many kinds of tools. Some of them were observed only at Bossou, and a few were only discovered 20 years after the establishment of Bossou as a research site. After decades of research on tool use in this species, I also suggested that there are cultural zones throughout the geographic distribution of chimpanzees.

     

The golden langurs (Presbytis geei Khajuria, 1956) of Assam

The ecology and behaviour of golden langurs,Presbytis geei Khajuria, 1956, were studied in the western forests of Assam. During our survey 10 groups were observed of which one was all male group and the rest were bisexual. Group composition, sex ratio of adult males and females, ratio of adult females to juveniles and infants, percentage of females with infants, number of males in each group, daily activity pattern, intra-inter group and inter-specific relations, reaction to disturbances, and vocalisation have been studied and included in this paper. The similiarity and differences in their behaviour from those of Hanuman langurs have been discussed.     

Determinants of female dispersal in Thomas langurs

Female dispersal occurs in a number of primate species. It may be related to: avoidance of inbreeding, reduction in food competition, reduction of predation risk, or avoidance of infanticide in combination with mate choice. Female dispersal was studied for a 5-year period in a wild population of Thomas langurs (Presbytis thomasi) that lived in one-male multi-female groups. Juvenile and adult individuals of both sexes were seen to disperse. Females appeared to transfer unhindered between groups, mostly from a larger group to a recently formed smaller one. They transferred without their infants and when not pregnant, and seemed to transfer preferentially during periods when extra-group males were harassing their group. During these inter-group encounters extra-group males seemed to try to commit infanticide. Thus, the timing of female transfer was probably closely linked to infanticide avoidance. Moreover, females seemed to transfer when the resident male of their group was no longer a good protector. The observations in the present study suggest that females transferred to reduce the risk of infanticide. Female dispersal may have another ultimate advantage as well, namely inbreeding avoidance. Due to the dispersal of both females and males the social organization of Thomas langurs was rather fluid. New groups were formed when females joined a male; male takeovers were not observed. Bisexual groups had only a limited life span, because all adult females of a bisexual group could emigrate. This pattern of unhindered female dispersal affects male reproductive strategies, and in particular it might lead to infanticidal behavior during inter-group encounters. Am. J. Primatol. 42:179–198, 1997. © 1997 Wiley-Liss, Inc.     

Seasonality of group size,feeding, and breeding in wild red‐shanked douc langurs (Lao PDR)

In Asian colobines, small one‐male groups (OMG) seem to predominate alongside all‐male groups (AMG), while larger multimale groups (MMG) are rare, but are reported for Hanuman langurs and red‐shanked douc langurs. Recently, however, it has been speculated that the genus Pygathrix could have multilevel societies based on (1) a theoretical extension of the multilevel societies found in Rhinopithecus to all odd‐nosed colobines and (2) first data for black‐shanked douc langurs. This assumes bands composed of small OMG with a skewed adult sex ratio. Band size may vary with seasonal food availability resulting in smaller bands when feeding competition is increased. To investigate the social organization of red‐shanked douc langurs and potential seasonal influences, we observed 2 unhabituated groups at Hin Namno National Protected Area, Lao PDR from March 2007 to August 2008 for 803 hr. We recorded births and performed group counts and scan sampling of feeding behavior. Most births (79% of N = 15) occurred from June–September, indicating a 4‐month peak conception season from November to February. Group size averaged 24.5 individuals (range 17–45) with 2.45 adult males (range 1–4). Although the smaller group remained at a stable size (about 18 individuals), the larger group reduced from about 45 to 25 individuals during the 7‐months long lean season, when less than 50% of the feeding time was spent on fruits. This suggests feeding competition as a potential cause of seasonal variation in group size. With 1.9 females per male the skew in adult sex ratio was much lower compared with Rhinopithecus, indicating MMG rather than multilevel societies. However, data on the spacing and interaction patterns between recognized individuals need to be collected and analyzed before the social organization can be determined. Detailed ecological data are furthermore required to investigate the basis for the seasonal changes in group size found. Am. J. Primatol. 73:1134–1144, 2011. © 2011 Wiley Periodicals, Inc.     

Factors influencing the population density of the hanuman langur (Presbytis entellus) in Sariska Tiger Reserve

We carried out a study of Hanuman langurs in Sariska Tiger Reserve, Rajasthan, India during three months in 1990. The area surveyed included habitat disturbed by human activity, with both the grazing of livestock and firewood collecting resulting in degraded forest. Langur population density was estimated to be between 19 and 36 animals/km². The density of langurs in disturbed areas was significantly lower than in undisturbed areas. Both tree cover, total tree, and shrub cover were positively correlated with langur density, suggesting that a lack of trees in disturbed areas may have caused the lower langur densities. Although bisexual groups were significantly more common in undisturbed areas the distribution of all male groups did not appear to be affected by human disturbance, suggesting that male bands are likely to inhabit more disturbed habitats than bisexual groups. We suggest that either a lack of food trees or the high density of predators in Sariska may prevent bisexual groups from inhabiting areas where tree cover is low, although the more mobile male groups can survive in these areas. Although Hanuman langurs are a relatively common species in India, these results suggest that they are not, as is commonly assumed, immune to the effects of human disturbance. In areas where langurs appear to survive in disturbed habitats the different response of bisexual and all male groups to disturbance may still result in serious disruption to the population structure.     

圈养白头叶猴春季昼夜活动节律

2008 年3 ～5 月,采用瞬时扫描法,对上海动物园5 只白头叶猴的行为进行24 h 昼夜连续观察。结果表明:春季圈养白头叶猴一天的活动起于06∶ 00 左右,结束于18∶ 00 或18∶ 30。白天白头叶猴的主要行为为休息、取食和移动,平均频次依次是13.79 次、4.75 次和2.18 次。夜间的主要行为为休息、移动和抓挠,平均频次依次是22.13 次、0.43 次和0.26 次。不同个体昼夜活动节律差异很大。其中,移动、理毛、玩耍和其它行为的差异显著。夜间无理毛和玩耍行为,移动行为在夜间21∶ 00, 00 ∶ 30, 03∶00 和04∶ 30 出现高峰。在22∶ 30, 01∶ 00, 02∶ 00, 03∶ 30, 04∶ 30 和05∶30 则出现抓挠高峰。这预示白头叶猴夜间休息时处于一个“轻睡眠”状态。同时,雌雄白头叶猴昼夜移动行为差异显著。     

Male monkeys remember which group members have given alarm calls

Primates give alarm calls in response to the presence of predators. In some species, such as the Thomas langur (Presbytis thomasi), males only emit alarm calls if there is an audience. An unanswered question is whether the audience's behaviour influences how long the male will continue his alarm calling. We tested three hypotheses that might explain the alarm calling duration of male Thomas langurs: the fatigue, group size and group member behaviour hypotheses. Fatigue and group size did not influence male alarm calling duration. We found that males only ceased calling shortly after all individuals in his group had given at least one alarm call. This shows that males keep track of and thus remember which group members have called.     

Down from the treetops: red langur (<Emphasis Type="Italic">Presbytis rubicunda</Emphasis>) terrestrial behavior

Using direct observations and camera traps at eight sites across Indonesian Borneo we show how red langurs (Presbytis rubicunda) are more terrestrial than previously believed, regularly coming to the ground. This unusual behavior has been found at six of the eight sites surveyed. We find that red langurs come to the ground more frequently in disturbed forests, specifically ones which have been impacted by logging, fire, and hunting, though more data are needed to confirm this as a direct correlation. We also found a trend towards decreased ground use with increased elevation of the habitat. When on the ground, red langurs are predominantly engaged in feeding (50% direct observations, 61% camera traps) and traveling (29% direct observations, 13% camera traps). Red langurs are found on the ground throughout the day, at similar times to activity periods of the apex predator, the Sunda clouded leopard (Neofelis diardi). We suggest that ground use by red langurs could be an adaptation to disturbed forest to exploit additional food sources and to facilitate travel.     

Seasonal Variation in the Activity and Dietary Budgets of Cat Ba Langurs (<Emphasis Type="Italic">Trachypithecus poliocephalus</Emphasis>)

Primate activity budgets are dictated by food availability and distribution; thus primates living in seasonal environments must adapt their behaviors to accommodate fluctuations in resources. Cat Ba langurs (Trachypithecus poliocephalus), a Critically Endangered Asian colobine and a member of the limestone langur group (francoisi superspecies group within genus Trachypithecus), live only in fragmented and disturbed habitats on Cat Ba Island, northeastern Vietnam. This study aimed to assess the behaviors and diet of Cat Ba langurs by group, age, sex, and season. We predicted they would have high rates of inactivity and foraging, low rates of social behaviors, with seasonal variation that reflects an energy-maximizing strategy. We conducted behavioral observations through scan sampling over an 11-month period and found that Cat Ba langurs spent a significant portion of their day inactive (57 %) followed by foraging (18 %), socializing (13 %), locomoting (10 %), and engaging in “other” behaviors (2 %). Their diet was made up primarily of leaves (83 %) followed by flowers (8 %), fruit (6 %), and stems (3 %). We found groups to differ in diet and activity, which is likely owing to differences in demographics and home range between groups. Seasonally, the animals ate more leaves and spent more time foraging in the dry season than the wet season, suggesting that they are energy maximizers. Cat Ba langurs have activity and dietary budgets similar to those of other limestone langurs, and respond to a presumed seasonal fluctuation in food availability similarly.     

Interspecific spacing between gibbons (Hylobates klossii) and langurs (Presbytis potenziani) on Siberut Island,Indonesia

Spatial arrangement and social interactions of two sympatric and ecologically similar primate species, Hylobates klossii and Presbytis potenzianai, are described from field observations made between July 1972 and October 1974 on Siberut Island, Indonesia. Gibbon territories and langur home ranges overlap extensively. Because gibbons have the ability to supplant langurs at shared food sources, langurs are at a competitive disadvantage. To avoid or decrease the frequency of hostile interactions with gibbons, langurs locate their core areas on boundaries between adjacent gibbon territories, which permits langurs to retreat across these barriers in response to gibbon movements. Langurs further enhance segregration by leaving their sleeping trees earlier than gibbons, gaining additional feeding time on contested food sources. This form of interspecific spatial organization between gibbons and langurs resembles certain predator-prey spacing systems, where territorial boundaries between adjacent predators serve as sanctuaries for prey populations.     

Social organization of white‐headed langurs (Trachypithecus leucocephalus) in the Nongguan Karst Hills,Guangxi, China

The number of males per group is the most variable aspect of primate social organization and is often related to the monopolizability of females, which is mainly determined by the number of females per group and their reproductive synchrony. Colobines show both inter‐specific and intra‐specific variations in the number of males per group. Compared with other colobine species, little is known about the social organization of white‐headed langur (Trachypithecus leucocephalus), despite its endangered status and unusual limestone habitat. As a part of a long‐term study of the white‐headed langurs in the Nongguan Karst Hills, Guangxi, China, we quantitatively investigated their social organization by analyzing census data from 1998 to 2003. The population censuses revealed that the predominant social organization of bisexual groups was the one‐male group, similar to a previous report on this species and many other Asian colobines. In such groups, one adult male associated with 5.1 adult females, 0.1 sub‐adult males, 2.6 juveniles and 2.9 infants on average, with a mean group size of 11.7 individuals. In addition, three multi‐male groups were recorded, consisting of 2–3 adult males, 1–5 adult females, 0–2 sub‐adult males, 0–7 juveniles and 0–2 infants. They did not contain more adult females than the one‐male groups and were unstable in group membership. The langurs outside bisexual groups were organized into small nonreproductive groups or lived as solitaries. The nonreproductive groups averaged 1.3 adult males, 1.3 sub‐adult males and 2.6 juveniles. Juvenile females were present in such groups on 52.4% of all occasions. As predicted by the monopolization model, the prevalence of the one‐male pattern in this species may mainly be attributed to the small number of females in the group. The possible reasons for the occurrence of multi‐male groups and the presence of juvenile females in nonreproductive groups are also discussed. Am. J. Primatol. 71:206–213, 2009. © 2008 Wiley‐Liss, Inc.     

Sex Allocation in a Colobine Monkey

In polygynous, sexual dimorphic species with higher variance in male reproductive success compared with females, females are expected to invest more heavily in sons than daughters within the constraints imposed by their physical condition (Science 1973; 179:90). Mothers in good condition, usually those of high rank, should produce more sons than females in poor condition or of low rank. We investigated sex allocation and sex‐biased maternal investment in a population of wild Hanuman langurs using rank and group size as approximations of female physical condition. Our results show that reproductive costs of sons were higher with both significantly longer interbirth intervals following male births and longer lactational periods for sons. Not in all groups did analyses of rank‐dependent sex allocation reveal the expected pattern of high‐ranking mothers producing more sons. However, sex ratio was significantly influenced by group size, with females from larger groups, i.e., in worse physical condition, producing a daughter‐biased sex ratio. In fact, only females of population‐wide superior physical condition can be expected to produce sons, because in Hanuman langurs males disperse and compete population‐wide. Thus, our results support the Trivers–Willard model and may explain the mixed evidence accruing from studies of single groups. We present a graphical model of how group size and dominance‐related differences in energy gain may influence sex allocation under different competitive regimes relative to overall resource availability. Tests of adaptive sex allocation models should consider whether reproductive competition of the preferred sex takes place primarily within a group or within the population.     

Analysis of a Nilgiri langur (Presbytis johnii) home range change

Little published information exists detailing home range changes among nonhuman primates. Resulting from human destruction of the habitat, one of the observed Nilgiri langur troops was forced to relocate its home range, during which several interesting behavioral patterns emerged. Most important was the observation that the animals were very reluctant to desert the home range, even when the last trees in the core area were being destroyed. Adult males and adult females responded differently to the destruction and resultant shift. The males appeared less nervous than the females and deserted the home range prior to them. The reaction of surrounding troops to the shift of troop A, strongly suggests territorial behavior among Nilgiri langurs. Finally, this shift, along with other observations reported elsewhere, demonstrates that Nilgiri langurs are quite adaptable and appear to possess the ability to survive in an ecology being rapidly destroyed by the human population.This study was supported by Public Health Service grant MH 11099-01 attached to Fellowship 2 F1-MH-22, 140-02 (BEH).     

Habitat Quality and Activity Budgets of White-Headed Langurs in Fusui,China

Within a species, habitat quality may be a factor causing different activity budgets between populations. The habitat of white-headed langurs (Trachypithecus leucocephalus) has been seriously disturbed in Fusui Rare and Precious Animal Nature Reserve, China, where we carried out a study of their socioecology from September 1997 to September 1998. We collected data on langur activity budgets from the main population located in the central part of a group of limestone hills. We classified habitat quality into 4 grades according to the extent of human disturbance. We showed that the two main study groups of white-headed langurs spent on average 50% of time resting, 13% feeding, 18% moving (including foraging), 11% grooming, and 7% playing. Langur time budgets showed no significant seasonal change, but they differed among different sex-age classes. Infants and juveniles spent about 20.3% of time playing, whereas adults spent only 0.2% playing. The group in high quality habitat engaged less in feeding and more in playing than the group in low quality habitat did. Habitat quality influenced the playing time of young white-headed langurs and may be vital to their successful maturation.     

DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys.

Although the killing of dependent infants by adult males is a widespread phenomenon among primates, its causes and consequences still remain hotly debated. According to the sexual selection hypothesis, infanticidal males will gain a reproductive advantage provided that only unrelated infants are killed and that the males increase their chances of siring the next infants. Alternatively, the social pathology hypothesis interprets infanticide as a result of crowded living conditions and, thus, as not providing any advantage. Based on DNA analyses of wild Hanuman langurs (Presbytis entellus) we present the first evidence that male attackers were not related to their infant victims. Furthermore, in all cases the presumed killers were the likely fathers of the subsequent infants. Our data, therefore, strongly support the sexual selection hypothesis interpreting infanticide as an evolved, adaptive male reproductive tactic.     

Sex Differential Behavior of Immature Hanuman Langurs (Presbytis entellus) in Ramnagar, South Nepal

We investigated sex differences in the social behavior of immature Hanuman langurs (Presbytis entellus) in the light of sex-specifically different life-courses and Hanuman langur characteristics, such as the individualistic dominance hierarchy and the rarity of intragroup coalitions among adult females. We observed four immature female and four immature male langurs—all members of the same free-ranging multimale multifemale group in Ramnagar, South Nepal—from November 1992 to February 1993 for 288 hr via focal-animal and instantaneous sampling techniques. Immature females spent significantly more time in proximity to other group members than immature males did. They had more physical contact and groomed more. Other immature females were their preferred social partners. Immature males also preferred like-aged females. They restricted their relationships with other immature males to proximity and occasional grooming. Monitoring was directed especially toward adult males. Female behavior can be interpreted as oriented toward integration into the female social network and their age-inverted dominance hierarchy. Males seem to prepare for leaving their natal group and for future strong intrasexual competition.     

Ranging and foraging of Himalayan grey langurs (Semnopithecus ajax) in Machiara National Park, Pakistan

Grey langurs (Semnopithecus spp.) occupy a variety of habitats, ranging from lowland forests and semi-desert to alpine forests. Little is known about their foraging and ranging in alpine forests, which appear to contain less food than lowland forests. We conducted a 1-year study of Himalayan grey langurs (Semnopithecus ajax) in Machiara National Park, Pakistan, where they occur at relatively high altitudes (range 2000–4733 m). We followed three groups of different sizes and compositions and examined the effects of ecological and social factors on ranging and feeding. The home-range sizes of a small bisexual group (SBG), a large bisexual group (LBG), and an all-male group (AMG) were 2.35 ± 0.92 (mean ± SD; average of four seasons), 3.28 ± 0.55, and 3.52 ± 1.00 km², respectively, and were largest in winter for all groups. The daily path lengths of the SBG, LBG, and AMG were 1.23 ± 0.28 (mean ± SD; average of four seasons), 1.75 ± 0.34, and 1.84 ± 0.70 km, respectively; that of the LBG was longer in winter, while that of the AMG was shorter in summer. Both the home-range size and daily path length of the AMG were larger than those of the other groups, even after partialling out the effect of group size differences. The mean altitude used by the langurs and the proportion of animals seen feeding did not differ among seasons or group types. As the mean temperature increased, the altitude used by langurs significantly increased for the SBG and LBG, but not for the AMG. On the other hand, as the temperature increased, the home-range sizes significantly decreased for the SBG and AMG, but not for the LBG. Rainfall did not show any correlation with ranging or feeding in any of the groups. Our results suggested that grey langurs in Machiara National Park employ a high-cost, high-return foraging strategy in winter, and that the ranging of the AMG also reflects its reproductive strategy.