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2018年  第39卷  第4期

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Over the past few decades, field studies conducted by Chinese primatologists have contributed significant new theoretical and empirical insights into the behavior, ecology, biology, genetics, and conservation of lorises, macaques, langurs, snub-nosed monkeys, and gibbons. With the recent establishment and inaugural meeting of the China Primatological Society in 2017, China has emerged as a leading nation in primate research. Several research teams have conducted long-term studies despite the difficult challenges of habituating and observing wild primates inhabiting mountainous temperate forests, and the fact that some 80% of China’s 25–27 primate species are considered vulnerable, endangered, or critically endangered and are distributed in small isolated subpopulations. In going forward, it is recommended that primatologists in China increase their focus on seasonal differences in the social, ecological, physiological, and nutritional challenges primates face in exploiting high altitude and cold temperate forests. In addition, provisioning as a habitation tool should be minimized or eliminated, as it is difficult to control for its effects on group dynamics, patterns of habitat utilization, and feeding ecology. Finally in the next decade, Chinese primatologists should consider expanding the taxonomic diversity of species studied by conducting research in other parts of Asia, Africa, and the Neotropics.
China is one of the most dynamic countries of the world and it shelters some amazing levels of biodiversity, including some very special primate species. However, primarily as a result of forest loss, most of which occurred in historical times, approximately 70% of China’s primate species have less than 3 000 individuals. Here I evaluate one road for future conservation/development that could produce very positive gains for China’s primates; namely forest restoration. I argue that for a large scale restoration project to be possible two conditions must be met; the right societal conditions must exist and the right knowledge must be in hand. This evaluation suggests that the restoration of native forest to support many of China’s primates holds great potential to advance conservation goals and to promote primate population recovery.
China supports the richest non-human primate diversity in the northern hemisphere, providing an excellent opportunity for Chinese primatologists to take a leading role in advancing the study of primatology. Primatology in China began to flourish after 1979. To date, Chinese primatologists have published more than 1000 papers in journals indexed by the Chinese Science Citation Database and the Web of Science Core Collection, and universities and academic institutions have trained 107 PhD students and 370 Masters students between 1984 and 2016. In total, the National Science Foundation of China has funded 129 primate projects (71.7 million Yuan) supporting 59 researchers from 28 organizations. However, previous research has also shown obvious species bias. Rhinopithecus roxellana, Rhinopithecus bieti, and Macaca mulatta have received much greater research attention than other species. Researchers have also tended to continue to study the same species (55.2%) they studied during their PhD training. To promote the development of primatology in China, we suggest 1) the need for a comprehensive primatology textbook written in Chinese, 2) continued training of more PhD students, and 3) encouragement to study less well-known primate species.
Gibbons in China represent the northernmost margin of present day gibbon species distribution (around N25°). Compared to tropical habitats, northern gibbon habitats are characterized by low temperatures and remarkable seasonal variation in fruit abundance. How gibbons adapt to their cold and seasonal habitats and what ecological factors affect their sociality are key questions for understanding their ecology and social system evolution, the elucidation of which will contribute to the conservation of these special populations/species. According to preliminary short-term studies, northern gibbons consume more leaves and use larger home ranges than tropical gibbons. Interestingly, some Nomascus groups consist of more than one adult female. However, these preliminary results are not well understood or incorporated into current socio-ecological theories regarding gibbon species. To better understand northern gibbons, our team has systematically studied three habituated groups of Nomascus concolor, three groups of N. nasutus, and two habituated groups of Hoolock tianxing since 2002. In this paper, we stress the challenges facing gibbons living in northern habitats and summarize their behavioral adaptations to their harsh environments. We also describe the northern gibbon social system and discuss the potential relationships between their ecology and sociality. Finally, we highlight future research questions related to northern gibbons in China.
In primate species with social systems consisting of one-male breeding units (OMUs), resident male takeover represents a major challenge to individual reproductive success and mating strategies. The golden snub-nosed monkey (Rhinopithecus roxellana) is characterized by large multilevel societies (MLS) comprised of several OMUs and all-male units (AMUs); however, the factors and mechanisms associated with resident male takeover, which offer important insight into primate reproduction and social strategies, are still poorly understood. Based on 5-year monitoring data from a free-ranging herd of golden monkeys from the Qinling Mountains in China, we categorized three phases of an OMU, that is, a rising phase, developing phase, and declining phase. The rising and declining phases were unstable periods in which male takeover in an OMU might occur. Factors causing takeover, such as leader male rank, fighting ability, reproduction rate, and affiliation (proximity, allogrooming), were analyzed for males and females and for different OMUs. Results indicated that the new resident male’s fighting ability was lower than that of the former resident male in 23 cases. After replacement, the rank order of the new resident male significantly declined. Females involved in a takeover increased their distance from the resident male and decreased mating frequency during the three months prior to takeover. Females with infants under one-year-old had a marked effect on the specific time of takeover occurrence. These results suggested that female choice was the main factor deciding whether a takeover attempt was successful. Furthermore, rather than male conflict, females more often initiated and affected takeover and outcome, implying that the social status and competitive ability of the males played lesser roles during takeover.
Play behaviors and signals during playful interactions with juvenile conspecifics are important for both the social and cognitive development of young animals. The social organization of a species can also influence juvenile social play. We examined the relationships among play behaviors, candidate play signals, and play bout termination in Tibetan macaques (Macaca thibetana) during juvenile and infant social play to characterize the species play style. As Tibetan macaques are despotic and live in groups with strict linear dominance hierarchies and infrequent reconciliation, we predicted that play would be at risk of misinterpretation by both the individuals engaged in the play bout and by those watching, possibly leading to injury of the players. Animals living in such societies might need to frequently and clearly signal playful intent to play partners and other group members to avoid aggressive outcomes. We gathered video data on 21 individually-identified juvenile and infant macaques (one month to five years of age) from the Valley of the Wild Monkeys, Mt. Huangshan, China. We used all-occurrence sampling to record play behaviors and candidate play signals based on an ethogram. We predicted that play groups would use multiple candidate play signals in a variety of contexts and in association with the number of audience members in proximity to the players and play bout length. In the 283 playful interactions we scored, juvenile and infant macaques used multiple body and facial candidate play signals. Our data showed that juvenile and infant Tibetan macaques use a versatile repertoire of play behaviors and signals to sustain play.
Comparative studies of sympatric species are essential for understanding behavioral and ecological adaptation as well as the mechanisms that can reduce resource competition to allow coexistence. François’ langurs (Trachypithecus francoisi) and Assamese macaques (Macaca assamensis) are sympatric primate species found in the limestone seasonal rainforests of Nonggang Nature Reserve, southwestern Guangxi, China. To explore their different adaptation strategies, we collected data on diet using scan sampling at 15-min intervals. Our results revealed that François’ langurs showed a more flexible diet composition than Assamese macaques. François’ langurs increased dietary diversity and mature leaf consumption in response to seasonal scarcity of preferred young leaves and fruits, whereas Assamese macaques relied heavily on young bamboo leaves (Indocalamus calcicolus) in most months. These variations reflect the differences in digestive physiology, morphology, and the temporal and spatial distribution of food resources.
The Tibetan macaque, which is endemic to China, is currently listed as a Near Endangered primate species by the International Union for Conservation of Nature (IUCN). Short tandem repeats (STRs) refer to repetitive elements of genome sequence that range in length from 1–6 bp. They are found in many organisms and are widely applied in population genetic studies. To clarify the distribution characteristics of genome-wide STRs and understand their variation among Tibetan macaques, we conducted a genome-wide survey of STRs with next-generation sequencing of five macaque samples. A total of 1 077 790 perfect STRs were mined from our assembly, with an N50 of 4 966 bp. Mono-nucleotide repeats were the most abundant, followed by tetra- and di-nucleotide repeats. Analysis of GC content and repeats showed consistent results with other macaques. Furthermore, using STR analysis software (lobSTR), we found that the proportion of base pair deletions in the STRs was greater than that of insertions in the five Tibetan macaque individuals (P<0.05, t-test). We also found a greater number of homozygous STRs than heterozygous STRs (P<0.05, t-test), with the Emei and Jianyang Tibetan macaques showing more heterozygous loci than Huangshan Tibetan macaques. The proportion of insertions and mean variation of alleles in the Emei and Jianyang individuals were slightly higher than those in the Huangshan individuals, thus revealing differences in STR allele size between the two populations. The polymorphic STR loci identified based on the reference genome showed good amplification efficiency and could be used to study population genetics in Tibetan macaques. The neighbor-joining tree classified the five macaques into two different branches according to their geographical origin, indicating high genetic differentiation between the Huangshan and Sichuan populations. We elucidated the distribution characteristics of STRs in the Tibetan macaque genome and provided an effective method for screening polymorphic STRs. Our results also lay a foundation for future genetic variation studies of macaques.