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30 January 2024, Volume 44 Issue 1

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ORIGINAL PAPERS

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Pelage colour change in Hainan gibbon (Nomascus hainanus)

ZHU Changyue, ZHONG Xukai, WANG Yuxin, LI Wenyong, QI Xuming, FAN Pengfei

2024, 44(1):  1-13.  DOI: 10.16829/j.slxb.150809

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All known species of the genus Nomascus have distinct sexual dichromatism in adulthood. The changes in their pelage colour are used as an important indicator of individuals’sexes, ages, and ontogenetic stages. This study is focused on Hainan gibbons (Nomascus hainanus), the rarest primate in the world, and combines the data of circa 2 years of continuous field observations and previously collected image data to describe the patterns of pelage colour changes over two crucial stages of their life history: natal coats to juvenile pelages and female fur colour changes during sexual maturity. The results show that monitoring and documenting the ‘crest’ traits, the overall fur colour, and the timing of colour change occurring at the different body parts could operatively assist in determining the age group of an individual, estimating the birth season of an infant, and identifying the fertile females in relatively complex environments, especially in dense rainforest. It was found that the development of the pelage colour change of N. hainanus in infancy was more similar to that of Cao Vit gibbon (Nomascus nasutus). This supports the latest and accepted phylogenetic position of Hainan gibbons. We also discussed the potential interpretations of the adaptation of their pelage colour change. We advocated that the practicable suggestions described in this study should be integrated with automated data collecting systems, which might help increase the efficiency and accuracy of the population monitoring and conservation of the endangered crested gibbons in the future.

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Spectral characteristics and sex differences in the song of Skywalker hoolock gibbon (Hoolock tianxing)

GUO Tingyan, MA Haigang, HAN Pu, WANG Zidi, ZHU Changyue, CHU Yuanmengran, ZHANG Lixiang, LI Ruxue, QI Jiaru, LI Jiahua, FAN Pengfei

2024, 44(1):  14-25.  DOI: 10.16829/j.slxb.150870

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Species of the genus Hoolock were previously thought to lack sexual dimorphism. Identifying sexual dimorphism in vocalizations is helpful for their population dynamics monitoring and behavioral research. In this study, we annotate the song bouts of 11 Hoolock tianxing individuals. We employed k-medoids clustering to divide note types, and we classified phrase types based on the length and note composition of phrases. We also compared sexual dimorphism in notes and phrases. We identified 5 note types: wa, oo, whoop, ow and eek. The range and rate of frequency modulation of wa and ow notes of females were higher than those of males, the frequency features of oo notes were lower than those of males, the range and rate of frequency modulation of whoop notes were lower than those of males. For the phrases use, solitary apes were more similar to the parts contributed by their respective genders during a chorus. Males seldom sing phrase G mainly composed of the whoop note and the ow note, females seldom sing phrase B (wa-whoop) and phrase C (wa-oo-wa-whoop). Our study demonstrated sexual dimorphism in the vocalizations of Hoolock tianxing, which is not only helpful for the monitoring of Hoolock tianxing, but also important for understanding the function of different note types and sex differences.

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The impact of climate on the birth pattern of Rhinopithecus roxellana in different regions

LU Zhantao, LAN Guanwei, LI Ruiyuan, SI Xurui, LIU Xingyu, MO Cheng, YAO Hui, QI Dun, XIANG Zuofu

2024, 44(1):  26-36.  DOI: 10.16829/j.slxb.150858

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The mating and reproduction of most non-human primates undergo strict seasonality, which are not only influenced by their own reproductive mechanisms, but also by the climate, altitude, and food supply in their habitats. Understanding the seasonal differences in the birth of the same primate species residing in different regions can help identify the impact of environmental variables on animal reproduction. From January 2023 to August 2023, by using focal animal sampling, we analyzed the relationship between climate and birth season in two groups of habituated Rhinopithecus roxellana populations in the Sichuan Baihe National Reserve (Baihe group) and the Dalongtan area in the Hubei Shennongjia National Park (Shennongjia group), China. The results showed that births occurred mainly between March and May in the two populations, but a few individuals were born in January, February, July, and August in the Baihe group. The birth patterns of the two groups were different, but the birth events were all distributed during periods of warming temperatures and rising precipitation. We detected a positive correlation between the weekly changes in infant / adult female values (I / F) and the weekly average temperature and precipitation in the Baihe group. The weekly variation of infant / adult female values (I / F) in the Shennongjia group is positively correlated with the weekly average temperature, but the correlation with weekly precipitation is not significant. The increase in temperature may be a factor in promoting the environmental response of pregnant female monkeys to childbirth, while precipitation can trigger reproductive events by affecting the food supply.

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Sleeping tree species selection and patterns of sleeping site use in a wild group of Yunnan snub-nosed monkeys (Rhinopithecus bieti) at Jinsichang, Lijiang, China

REN Baoping, WU Ruidong, LI Dayong, Paul A. Garber, LI Ming

2024, 44(1):  37-49.  DOI: 10.16829/j.slxb.150813

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Studies of sleeping site use in wild primates offer insights into species-specific patterns of ranging and habitat utilization. From December 2003 to October 2004, we recorded sleeping site use in a wild group of 180 Yunnan snubnosed monkeys (Rhinopithecus bieti) at Jinsichang, Lijiang City, Yunnan Province, China. A programmed auto-released GPS collar was used to track the movements of the monkeys. We obtained 272 GPS nighttime locations and visually confirmed 131 sleeping sites within the group’s 17. 8 km² home range. Seventy (53. 4%) sleeping sites were used on only one occasion, whereas the remaining 61 (46. 6%) were used between 2 and 9 times over the 11-month tracking period. On three occasions the monkeys slept in the same site during three consecutive nights and on 16 occasions they reused the same sleeping site on two consecutive nights. Re-use of sleeping areas over consecutive nights accounted for only 7. 0% of our sample and principally occurred during the winter months of November-April (84. 0% compared to the rest of the year). The average time interval between the reuse of the same sleeping site was 50 days. Daily travel distance was significantly shorter (527 m vs. 884 m) when sleeping sites were reused on consecutive nights. Sleeping sites of Yunnan snub-nosed monkeys were used in relation to their proximity to late afternoon and next day early morning feeding sites. Given the large size of the snub-nosed monkey group, we argue that limited reuse of sleeping sites represents a pattern of habitat exploitation characterized by the avoidance of recently visited areas and a foraging strategy of searching for scattered but highly productive feeding sites that are widely distributed across their home range. Furthermore, the monkeys highly selected Himalayan hemlock (Tsuga dumosa) as sleeping trees and rarely fed in trees that were used as sleep nighttime sleeping sites.

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The relationship between grooming behavior and parasite infections in wild Tibetan macaques

ZHANG Jie, CHEN Shiwang, TIAN Hongwei, SUN Binghua, WANG Xi, XIA Dongpo

2024, 44(1):  50-57.  DOI: 10.16829/j.slxb.150856

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Social grooming is the most extensive and frequent social interaction pattern within non-human primates, while accumulating evidence points that social grooming is not a low-cost investment given the potential health risks associated with parasite infection during the grooming process. This study aimed to investigate the potential health costs of social grooming by estimating the associations between the amount of social grooming given and the type and infection risk of parasites in wild Tibetan macaques (Macaca thibetana) in MT. Huangshan, Anhui Province, China. Our results showed that a total of 11 species of parasites were found, the highest risk of infection is the Capillaria spp. / Trichostrongylus spp. and Balantidium coli (93%), followed by the Trichuris trichura (54%). As the durations of social grooming initiated increased, the higher the risk of infection with Balantidium coli, while the risk of infection with Ascaris spp. decreased with the increase in social grooming received. In addition, we noted that the risk of infection with Balantidium coli also showed an increasing tendency with the node strength increase in social grooming networks. In general, our results provided empirical evidence for the risk of parasite infections in wild Tibetan macaques, while also offering a new perspective on the trade-off between the benefits and costs of social grooming in non-human primate societies.

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Effects of month age and sex on mother - infant relationship in whiteheaded langurs (Trachypithecus leucocephalus)

LI Jiaxing, ZHOU Yingming, HUANG Chengming, FAN Penglai, ZHOU Qihai

2024, 44(1):  58-64.  DOI: 10.16829/j.slxb.150784

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Mother-infant relationship of non-human primates is the first social experience in their lifetime, which is very important to infants. This relationship is of great significance to the growth and development, normal social behavior and mental health of infants. Therefore, it respresents one of the hotspots in primatology research. In order to understand the development of the mother-infant relationship of the white-headed langur (Trachypithecus leucocephalus) and it’s influencing factors, data on the mother-infant relationship were collected from a wild group of white-headed langurs in the Bapen area of the Chongzuo White-headed Langur National Nature Reserve, Guangxi, between September 2009 and August 2010. The duration and frequency of mother-infant behavior were recorded. Combining with the month age and sexes of infants, we explored the effects of different ages and sexes of infants on the mother-infant relationship of white-headed langurs. The results showed that the mother-infant relationship of white-headed langurs was influenced by the month age of infants. The duration of mother-infant behavior was not affected by the sex of infants, but mothers cared for female infants significantly more frequently than male infants. The sex of infants has no effect on grooming behavior and lactating behavior between mothers and infants, but it has a significant effect on embracing behavior between mothers and infants. These results indicate that the infant’s development is a process from dependence on the mother to gradually integrating into the community independently. White-headed langur mothers take different care modes for male and female infants, which may be related to the different social roles of male and female infants in the future.

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Sexual interference in Taihangshan macaque (Macaca mulatta tcheliensis), Jiyuan, north China

HAN Mengya, TIAN Jundong, ZHOU Yanyan, WANG Yuwei, LUO Tongtong, LU Jiqi

2024, 44(1):  65-76.  DOI: 10.16829/j.slxb.150818

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Sexual interference refers to the phenomenon in which an animal is disrupted during mating by other individuals of the same species through various means such as chemical pheromones, facial expressions, sounds, and aggression. Sexual interference behavior, a significant topic in ecological studies of reproductive behavior in non-human primates, exhibits considerable inter- and intraspecific variation. Within species, it is primarily influenced by factors such as sex and age. The present study was conducted in the Wulongkou area of Taihangshan Macaque National Nature Reserve, focusing on the WLK-1A group of Taihangshan macaques. From September 2021 to August 2022, we observed and recorded the mating behaviors of the target individuals by using the focal animal sampling method and the continuous recording method with the expectation of exploring the sexual interference behaviors and their age-sex group differences in Taihangshan macaques. The results showed that (1) sexual interference behavior of Taihangshan macaques only occurred in the mating period, with the peak in November; (2) From the perspective of the initiators of sexual interference, male (adult and sub-adult) individuals accounted for 29. 1%, female (adult and sub-adult) individuals accounted for 14. 9%, juvenile individuals accounted for 7. 5%, and infant individuals accounted for 48. 5%; (3) Both male (P =0. 011) and female (P = 0. 033) interrupters used mainly non-contact harassment, while there was no significant difference between the non-contact and contact harassment in juvenile interrupters (P = 0. 334), and infant interrupters used mainly contact harassment (P = 0. 001); (4) Male interrupters tended to interrupt the females in the mating pairs (P = 0. 040). There was no significant difference in the harassment frequency of female interrupters toward males and females of the mating pairs (P = 0. 157). Sexual interference by juveniles mostly pointed to their mothers (90%) and that by infants all pointed to their mothers. The frequencies, patterns, and targets of sexual interference in Taihangshan macaques show age-sex group differences. Based on functional analysis, this study concludes that sexual interference in both adult males and females supports the sexual competition hypothesis, that in juveniles supports the learning hypothesis, and that in infants supports the separation anxiety hypothesis and learning hypothesis. The results of this study help increase the understanding of the development of sexual interference behavior and its functional differences in non-human primates.

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The parameters and pattern of copulation behaviors in Taihangshan macaque (Macaca mulatta tcheliensis), Jiyuan, China

HE Minqiang, TIAN Jundong, LI Wentao, LU Jiqi

2024, 44(1):  77-84.  DOI: 10.16829/j.slxb.150860

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Survival and reproduction are the nature of animals, and copulation is the key process of sexually reproducing animals, which could be shaped by natural selection and sexual selection. However, it is difficult to observe copulation in the wild, and therefore there is lack of quantitative analyses of wildlife’copulation. In this study, a troop of free-ranging Taihangshan macaques (Macaca mulatta tcheliensis) was assigned as the study object, and the data of copulation was collected through focal-animal sampling and analyzed within the Macaca genus. The results showed that, (1) the social grooming (49. 8%) was the dominant pre-copulation behavior and initiated by adult females (61. 8%); (2) a copulation cycle was composed of 12 mounting bouts and a successful ejaculation, lasting (719. 4 ± 43. 3) s on average, and the copulation pattern of Taihangshan macaque could be classified as multiple-mount-to-ejaculation pattern; (3) social grooming (19. 4%) and resting (18. 1%) were the main behaviors during the post-copulation period, and the copulation bond could last (2. 1 ± 2. 03) d; (4) the copulation patterns of used macaque species were consistent with the phylogenetic relationship and the traditional taxonomic classification rather than with social style, while the copulatory parameters varied among species. This study quantitatively analyzed the copulatory behaviors, and the copulation patterns of macaque species were relatively conserved according to the phylogenetic relationship and traditional taxonomic classification.

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Distribution and conservation status of Lorisinae primates in the middle and lower reaches of Nanxi River in southeastern Yunnan

ZHAO Kairui, LIAO Linhong, XIE Lei, DU Yating, DONG Pengmei, XIE Meng, NI Qingyong

2024, 44(1):  85-93.  DOI: 10.16829/j.slxb.150859

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The Bengal slow loris (Nycticebus bengalensis) and the pygmy loris (Xanthonycticebus intermedius) are two species of Lorisinae primates recorded in China. Their unique ecological and behavioral characteristics highlight the importance of research and conservation. However, they are continuously threatened by hunting and habitat loss, resulting in declining populations and shrinking distribution areas. The lack of population and distribution data has hindered the development and implementation of conservation plans. Southeastern Yunnan is a vital region historically known for the presence of Lorisinae primates and the potentially sympatric range of both species. From October 2022 to September 2023, we conducted a detailed assessment of this taxon’s distribution and conservation status in Hekou and Maguan counties by interview and transect surveys. We identified nine forest areas with high encounter rates of loris primates. The results showed that this region remains essential for Lorisinae distribution, especially for the pygmy loris. The local communities have a relatively low level of awareness and knowledge about this taxon, which is significantly influenced by education, age, and economic conditions. The distribution areas of loris primates are mainly located on the edges of nature reserves, and current protection approaches seem to be unreliable. It is urgent to strengthen monitoring and management, establish ecological corridors, and raise awareness among local communities through outreach and education programs.

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The body weight of wild Tibetan macaques (Macaca thibetana) and its influencing factors

SUN Yu, XIA Mengyi, XIA Yingna, WANG Jingjing, LU Jiakai, LIU Shenqi, XIA Dongpo, WANG Xi, SUN Binghua

2024, 44(1):  94-102.  DOI: 10.16829/j.slxb.150861

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Body weight is an important indicator of primate life history and growth and development characteristics, which can suggest information about the physiological condition, behavioral changes, and ecological adaptations of animals. In this study, we monitored the body weights of 48 Tibetan macaques (Macaca thibetana) from the YA1 group in the Wild Monkey Valley of Huangshan Mountain, Anhui Province, for 11 consecutive months (July 2022 to May 2023) using floor scales. The mean body weight of male Tibetan macaques (18. 71 ± 2. 33) kg was significantly higher than that of females (11. 79 ± 1. 97) kg, and the rapid development of body weight occurred between 3 and 5 years old in males and between 2 and 3 years old in females. There was a significant positive correlation between body weight and individual social rank in both adult males and females (P <0. 001). There was significant seasonal variation (P <0. 05) in body weights of adult Tibetan macaques, with both males and females having their highest body weights in autumn, but males having their lowest body weights in winter and females having their lowest body weights in spring. The body weights of non-pregnant individuals did not differ significantly between seasons, whereas the body weights of pregnant individuals decreased significantly (P <0. 05) from winter to spring. The present study showed that there was a significant male-female dimorphism in body weight, a significant differentiation in the rapid developmental period of immature body weight, and a significant effect of both season and social rank on body weight in Tibetan macaques.

REVIEWS

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The roles of color signals in the sexual selection of non-human primates

LIN Jinhuang, YAO Hui, WU Feng, XIANG Zuofu

2024, 44(1):  103-117.  DOI: 10.16829/j.slxb.150757

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The phenotypic coloration of animals is polychrome which includes plumage, pelage, and skin. It plays an important role in intraspecific communication, predation defense, and thermoregulation. The role of phenotypic coloration in sexual selection deserves to receive considerable critical attention. Non-human primates are an excellent model for investigating the role of phenotypic coloration in sexual selection, owing to their varied and complex pelage and bare skin coloration, mating systems, and visual systems. However, few studies on this subject were conducted in China. Based on a review of studies on the role of phenotypic coloration under sexual pressure in non-human primates, we found that intersexual selection prefers brightly colored individuals due to potential health conditions, while intrasexual color is more likely to represent rank and individual competitive desire. Mandrills (Mandrillus sphinx) and rhesus macaques (Macaca mulatta) are the main study subjects in skin coloration studies. The color signal is analyzed in most studies but pelage coloration is rarely involved. Overall, the physiological mechanisms and genetic expression related to phenotypic coloration need to be further explored. Visual model is a more accurate color signal receiving method than spectroscopy and digital photography, but digital photography is a more convenient and operable method in most of the current research conditions.

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Advances in personality research in non-human primates

LI Nianlong, ZHAO Haitao, LI Wei, WANG Xiaowei, WANG Chengliang, MOU Junjie, LI Baoguo

2024, 44(1):  118-128.  DOI: 10.16829/j.slxb.150747

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The study of personality has deepened people’s understanding of individual differences and social organization patterns among group-living animals, making it a hot topic for primatologists and providing new avenues for studying the intersection of social psychology and behavioral ecology. This paper briefly summarizes the definitions, assessment methods, and advances in current primate personality research. Notably, this paper discusses the mechanism of personality formation in terms of hormonal changes, loci-specific differences, and environmental conditions, as well as the function of personality in individual health and cognition, to enhance primate welfare and management. Further exploration of behavioral ecology theoretical questions related to the personalities of primate species is needed. Researchers also need to further explore the personalities and behavioral patterns of individuals in the wild, suggesting in-depth studies on sexual selection, community structure, and spatial dynamics to effectively propose new concepts for endangered species conservation.

SCIENTIFIC NOTES

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Preliminary study on the conflict behavior between sympatric Hainan gibbons and rhesus macaques in the National Park of Hainan Tropical Rainforest

CAI Chenglin, LIU Shuai, LI Ping, QI Xuming, ZHOU Zhaoli, CHEN Yuan, LONG Wenxing

2024, 44(1):  129-134.  DOI: 10.16829/j.slxb.150855

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Understanding the pattern and the process of interspecific competition among sympatric animals is important, as interspecific competition is a key factor limiting population increase and is of great significance for conservation management. Hainan gibbon (Nomascus hainanus) is one of the most endangered primates in the world, currently distributed only in the Bawangling area of National Park of Hainan Tropical Rainforest, Hainan, China. Rhesus macaque (Macaca mulatta) population, a common species in this area, is growing rapidly in recent years, which may lead to interspecific competition with Hainan gibbons. In this study, we used focal animal sampling and whole-event recording methods to investigate the conflict behavior between one gibbon group (Group E) and one macaque group. Based on the observation of individuals and food patches, we inferred the recorded conflict behavior between these two species was a case of interference competition. Our results provided an important case for understanding the processes and mechanisms of primate interspecific relationships. This study emphasizes that the effects of interspecific competition should be fully recognized in the conservation management of endangered species.