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Data on the gut microbiota of animals can provide new insights into dietary ecology of hosts, consequently assisting in understanding their adaptation strategy and evolutionary potential. We studied the gut microbiota composition and function of the wild rhesus macaques (Macaca mulatta) using 16S rRNA sequencing method. Our results revealed that the gut microbiota of the wild rhesus macaques was dominated by Firmicutes, Bacteroidetes, and Spirochaetes. Diversity and richness of gut microbiota were higher during the dry season than the rainy season. Specifically, higher proportions of Firmicutes, Tenericutes, Cyanobacteria, and unclassified bacteria at the phylum level and more Coprococcus at the genus level were detected in the dry season. Predictive functional analysis showed that pathways associated with carbohydrate metabolism and drug resistance (antimicrobial and antineoplastic) were richer in the dry season. These seasonal differences in microbiota could be due to their heavier dependence on leaf-based diet in the dry season. Additionally, macaques in limestone forests had a higher percentage of Spirochaetes, probably suggesting that the proportion of fruits in dietary composition also play an important role in the gut microbiota. We concluded that diet was strongly linked to the diversity, composition, and function of the gut microbiota in the wild groups of rhesus macaques living in the limestone forest, highlighting the importance of diet in the gut microbiota of macaques and the need to conduct further study on the adaptation strategy in response of environmental changes in the ground of gut microbiota.
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Biodiversidade , Microbioma Gastrointestinal/genética , Macaca mulatta/microbiologia , Estações do Ano , Animais , Bactérias/classificação , Bactérias/genética , China , Dieta , Florestas , RNA Ribossômico 16S/genéticaRESUMO
The feeding posture of a group of François' langurs in Fusui County, Guangxi, was studied using instantaneous scan sampling from January to December 2016 to explore how the species adapts to karst limestone forests by collecting data on feeding posture, forest strata height, and substrate use. The results showed that leaves were the main food type of the François' langurs, with young leaves accounting for 64.97% ± 19.08% of the food composition, mature leaves accounting for 11.88% ± 12.09%, fruits accounting for 12.96% ± 12.89%, flowers accounting for 4.16% ± 4.06%, and other food types, including stems, petioles, and other unknown parts of the tree, accounting for a total of 6.03% ± 9.09%. The François' langurs had four main postures during feeding, of which sitting and bipedal standing feeding accounted for the largest proportions, at 85.99% ± 5.97% and 12.33% ± 6.08% of the total records, respectively. Quadrupedal standing and suspending were rarely observed and only appeared occasionally during feeding activities at the peak resting period, the two postures together accounting for 1.39% ± 1.59% of the total records. The feeding postures of the langurs had marked seasonal variation, as evidenced by the fact that seated feeding accounted for a significantly higher proportion of the total behavioral records in the rainy season than in the dry season, whereas feeding while standing bipedally was significantly more frequent during the dry season. Correlation analyses showed that feeding posture was correlated with food composition, showing a positive correlation between the proportion of bipedal standing feeding and mature leaf consumption. François' langurs preferred to forage in the lower and middle forest layers, with the lower forest layer accounting for 55.93% ± 16.50% of the total number of recordings and the middle forest layer accounting for 33.63% ± 18.33%. Langurs were less likely to forage on the ground (rocks), accounting for only 6.79% ± 4.78% of the records. The frequency of langurs feeding in the upper part of the forest layer was the lowest at 3.65% ± 2.73%. Additionally, in the dry season, langurs utilized the lower forest layer more but used the middle forest layer less than in the rainy season. This study demonstrates that the spatial distribution of foods in the limestone forest has an important effect on the feeding posture of François' langurs and their forest layer utilization.
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The coevolution between gut microbiota and the host markedly influences the digestive strategies of animals to cope with changes in food sources. We have explored the compositional structure and seasonal variation in the gut microbiota of François' langur in a limestone forest in Guangxi, southwest China, using 16S rRNA sequencing. Our results demonstrated that Firmicutes and Bacteroidetes were the dominant phyla in langurs, followed by Oscillospiraceae, Christensenellaceae, and Lachnospiraceae at the family level. The top five dominant phyla did not show significant seasonal variations, and only 21 bacterial taxa differed at the family level, indicating stability in gut the microbiota possibly with respect to foraging for several dominant plants and high-leaf feeding by the langurs. Moreover, rainfall and minimum humidity are important factors affecting the gut microbiota of the langurs, but they explain few changes in bacterial taxa. The activity budget and thyroid hormone levels of the langurs did not differ significantly between seasons, indicating that these langurs did not respond to seasonal changes in food by regulating behavior or reducing metabolism. The present study indicates that the gut microbiota's structure is related to digestion and energy absorption of these langurs, providing new perspectives on their adaptation to limestone forests. IMPORTANCE François' langur is a primate that particularly lives in karst regions. The adaptation of wild animals to karst habitats has been a hot topic in behavioral ecology and conservation biology. In this study, gut microbiota, behavior, and thyroid hormone data were integrated to understand the interaction of the langurs and limestone forests from the physiological response, providing basic data for assessing the adaptation of the langurs to the habitats. The responses of the langurs to environmental changes were explored from the seasonal variations in gut microbiota, which would help to further understand the adaptive strategies of species to environmental changes.
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Microbioma Gastrointestinal , Presbytini , Animais , Estações do Ano , Carbonato de Cálcio , RNA Ribossômico 16S/genética , China , FlorestasRESUMO
The white-headed black langur (Trachypithecus leucocephalus) is exclusively distributed in the karst forests and is critically endangered owing to habitat fragmentation. Gut microbiota can provide physiological data for a comprehensive study of the langur's response to human disturbance in the limestone forest; to date, data on spatial variations in the langurs' gut microbiota are limited. In this study, we examined intersite variations in the gut microbiota of white-headed black langurs in the Guangxi Chongzuo White-headed Langur National Nature Reserve, China. Our results showed that langurs in the Bapen area with a better habitat had higher gut microbiota diversity. In the Bapen group, the Bacteroidetes (13.65% ± 9.73% vs. 4.75% ± 4.70%) and its representative family, Prevotellaceae, were significantly enriched. In the Banli group, higher relative abundance of Firmicutes (86.30% ± 8.60% vs. 78.85% ± 10.35%) than the Bapen group was observed. Oscillospiraceae (16.93% ± 5.39% vs. 16.13% ± 3.16%), Christensenellaceae (15.80% ± 4.59% vs. 11.61% ± 3.60%), and norank_o__Clostridia_UCG-014 (17.43% ± 6.64% vs. 9.78% ± 3.83%) were increased in comparison with the Bapen group. These intersite variations in microbiota diversity and composition could be accounted for by differences in food resources caused by fragmentation. Furthermore, compared with the Banli group, the community assembly of gut microbiota in the Bapen group was influenced by more deterministic factors and had a higher migration rate, but the difference between the two groups was not significant. This might be attributed to the serious fragmentation of the habitats for both groups. Our findings highlight the importance of gut microbiota response for the integrity of wildlife habitats and the need in using physiological indicators to study the mechanisms by which wildlife responds to human disturbances or ecological variations.
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Assessment of gut microbiota, used to explore ecological adaptation strategies and evolutionary potential of species, provides a new viewpoint to the conservation and management of endangered animals. In this research, the gut microbiota of a group of semiprovisioned rhesus macaques (Macaca mulatta) living in a limestone forest exhibiting seasonal changes in plant items were studied to investigate the adaptation strategies of these macaques to this specific habitat. The findings revealed significant seasonal changes in the diversity and composition of the rhesus macaques' gut microbiota, which were higher in the rainy season than in the dry season. In the rainy season, Bacteroidetes (31.83 ± 16.14% vs. 19.91 ± 18.20%) were significantly increased and Prevotella (23.70 ± 15.33% vs. 15.40 ± 16.10%), UCG-002 (4.48 ± 3.16% vs. 2.18 ± 2.01%), and UCG-005 (4.22 ± 2.90% vs. 2.03 ± 1.82%) were more enriched at the genus level. In the dry season, Firmicutes significantly increased (71.84 ± 19.28% vs. 60.91 ± 16.77%), and Clostridium_sensu_stricto_1 (8.45 ± 9.72% vs. 4.76 ± 6.64%), Enterococcus (10.17 ± 13.47% vs. 0.69 ± 2.36%), and Sarcina (4.72 ± 7.66% vs. 2.45 ± 4.71%) were more enriched at the genus level. These differences in gut microbiota may be due to seasonal variations in plant items in these habitats alongside changes in the provisioned foods from tourists. Additionally, deterministic processes predominate the assembly of the macaque's gut microbiota community. This indicates that the animal's high reliance on natural plants and provisioned foods increased the impact of deterministic processes. This study concludes that a balance between provisioned foods and natural plants might be vital in shaping the gut microbiota in the macaques. Furthermore, the dynamic adjustment in gut microbiota might be a physiological mechanism for the macaques in response to the seasonal variations in the ecological factors and food provision.
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Understanding how animals cope with habitat-specific environmental factors can assist in species conservation management. We studied the habitat use of four groups (two large and two small groups) of white-headed langurs (Trachypithecus leucocephalus) living in the forest of southwest Guangxi, China between September 2016 and February 2017 via instantaneous scan sampling. Our results showed that the langurs primarily used hillsides (55.91% ± 6.47%), followed by cliffs (29.70% ± 5.48%), hilltops (7.26% ± 3.55%), flat zones (6.99% ± 6.58%), and farmlands (0.14% ± 0.28%). The langurs moved most frequently on hillsides (49.35% ± 6.97%) and cliffs (35.60% ± 9.17%). The hillsides were more frequently used (66.94% ± 7.86%) during feeding, and the langurs increased the use of hilltops during the rainy season, and the use of cliffs in the dry season. The langurs frequently rested on hillsides (49.75% ± 8.16%) and cliffs (38.93% ± 8.02%). The larger langur group used cliffs more frequently when moving and resting, whereas the small langur group used hillsides more frequently while resting. Langurs in all groups avoided the flat zones for feeding. Their use of habitat reflected the balancing of foraging needs, thermoregulation, and predator avoidance. We conclude that the ecological factors are determinants of habitat use for white-headed langurs. Our findings suggest that conservation efforts should focus on protecting the vegetation on the hillsides and restoring the vegetation on the flat zones.
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Host characteristics, such as sex and age, are closely associated with the structure and function of gut microbiota; however, less is known about the effects of age and sex on the gut microbiota of nonhuman primates, and therefore, our knowledge of interindividual variability in host gut microbiota is limited. In this study, 153 fecal samples from rhesus macaques (Macaca mulatta) were analyzed using high-throughput 16S rRNA sequencing in order to explore associations between age and sex of the host and their gut microbiota. The results indicated that female macaques had higher alpha diversity and a more unique gut microbiota than did males. The proportion of Proteobacteria, Tenericutes, Cyanobacteria, unclassified bacteria, and Verrucomicrobia was higher in females than that in males. We also found that adults of both sexes had a higher alpha diversity, a higher proportion of norank Ruminococcaceae, Oscillospira, norank Lachnospiraceae, norank Clostridiales, and Succinivibrio, and a lower proportion of Enterococcus than immatures. Functional analyses revealed that the richness of metabolic pathways was higher in females than males and in adults compared with immatures. These results could be attributed to differences in the nutritional requirements and hormone levels of macaques of different sex and age classes. We conclude that variation in the gut microbiota of different sex and age classes of rhesus macaques may be linked to age- and sex-specific differences in nutrient requirements and hormone levels. These results highlight the importance of host age and sex on the structure and function of the gut microbiota and the need to consider physiological traits when conducting studies on the gut microbiota.
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Food habits are important factors in the adaptation of wild nonhuman primates. White-headed langurs (Trachypithecus leucocephalus) are endemic to heavily fragmented limestone forests and adapt to unique living environments via flexible food selection strategies. In this study, we compared the dietary data for white-headed langurs living in Chongzuo White-headed Langur National Nature Reserve in 2013 and 2016 to evaluate interannual variations in diet. Our results indicated that young leaves were the main food source for langurs, accounting for 52.4% (SD 25.4%) and 65.2% (SD 22.4%) of their diet in 2013 and 2016, respectively. The pattern of plant part consumption was similar between the two years. The consumption of young leaves varied with the availability of young leaves, whereas the consumption of mature leaves was negatively correlated with young leaf availability. The consumption of plant species and diet diversity were higher in 2013 than in 2016. In both 2013 and 2016, although diet diversity varied with the consumption of mature leaves, it was negatively correlated with the consumption and availability of young leaves. Dietary interannual variation is likely to either be linked to phenological variations or indicate that white-headed langurs have a flexible ecological adaptation coping with habitat fragmentation.
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Information on positional behavior contributes to the understanding of the ecological adaptation mechanisms in animals. We collected data on the positional behavior of white-headed langurs (Trachypithecus leucocephalus) at the Guangxi Chongzuo White-Headed Langur National Nature Reserve from September 2016 to August 2017 via instantaneous scan sampling method. This study aimed to examine the importance of positional behavior flexibility in limestone forests characterized by seasonal variations in climate and food resources. Our results indicated that langurs adopted leaping (47.92% ± 5.50%) and vertical climbing (40.13% ± 6.20%) as their predominant locomotor modes and sitting (83.08% ± 4.70%) as their predominant posture. Their positional behavior exhibited marked seasonal variations. More specifically, langurs used quadrupedal walking more frequently during the dry season than during the rainy months. In the stationary state, they sat more frequently during the dry season, whereas they laid and suspended more often during the rainy season. Their positional behavior was affected by fruit availability, day length, and temperature. Quadrupedal walking increased with the decrease in fruit availability, whereas leaping was positively correlated with fruit availability. Moreover, sitting was positively correlated with average temperature but negatively correlated with day length. Lying was also negatively correlated with temperature but positively correlated with day length. We conclude that white-headed langurs adapt to limestone forests with positional behavior flexibility in response to seasonality. Our research provides evidence of the effects of food availability, ambient temperature, and day length on the positional behavior of white-headed langurs, highlighting the need to understand their behavioral ecology and the influence of ecological factors on behavioral adaptation.
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Climatic factors such as temperature and humidity vary seasonally in primate habitats; thus, behavioral adjustments and microhabitat selection by primate species have been interpreted as behavioral adaptations. François' langur (Trachypithecus francoisi), a native species to southwest China and northern Vietnam, inhabits a limestone habitat with extreme climatic conditions. To understand the potential effects of climatic seasonality on this species, we collected data on the individual behavioral budgets in a T. francoisi group between January and December 2010 in Fusui County, China. Monthly, we performed 5-11 days of observation during this period, using focal animal sampling and continuous recording methods. We also recorded ambient temperature (T a) and relative humidity (H r) data at our study site. Results indicated that T a and H r were significantly correlated with each other and fluctuated dramatically on a daily, monthly, and seasonal basis. The amount of time spent resting, grooming, basking, and huddling also varied on a daily, monthly, and seasonal basis. The proportion of resting time and total sedentary activity time significantly increased at high and low T as, respectively. The total sedentary time, resting time, and plant branch use all showed positive significant correlations with T a. Our results suggest that behavioral adjustment and support use of T. francoisi, at least partly, were related to thermoregulation. T. francoisi minimized thermal stress through behavioral adjustments and support use. It is an adaptive behavior associated with the climatic extremes of limestone habitat. This study can potentially advise conservation management strategies in this specific habitat. Conservation efforts should focus on vegetation restoration in langurs' habitat, including those in the foothills.
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The gut microbiota plays an important role in animal health and is strongly affected by the environment. Captivity and human source food have been shown to influence drastically the gut microbiota composition and function of wild animals. Therefore, in the present study, the gut microbiota of provisioned and wild populations of limestone-living rhesus macaques (Macaca mulatta) were compared using high-throughput 16S rRNA sequencing and bioinformatic analyses. The results indicated that provisioned macaques had a higher microbial richness than wild macaques, but there was no significant difference in the evenness of the gut microbiota between the two populations. Provisioned macaques also showed a higher abundance of Firmicutes and a lower abundance of Bacteroidetes than wild macaques. Functional analysis revealed that wild macaques had enriched microbial pathways involved in glycan biosynthesis and metabolism, transport and catabolism, and the digestive and endocrine systems, while provisioned macaques were richer in pathways associated with signaling molecules and interaction, neurodegenerative diseases. These differences were likely due to modification of the gut microbiota of the provisioned macaques to enable the digestion of new foods.
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Carbonato de Cálcio , Florestas , Microbioma Gastrointestinal , Macaca mulatta , Ração Animal , Animais , Biodiversidade , China , Sequenciamento de Nucleotídeos em Larga Escala , Humanos , Metagenoma , Metagenômica/métodos , RNA Ribossômico 16S/genéticaRESUMO
Determining the nutrient factors influencing food choice provides important insight into the feeding strategy of animals, which is crucial for understanding their behavioral response to environmental changes. A bamboo-leaf-based diet is rare among mammals. Animals' food choice and nutritional goals have been explained by several frameworks; however, the influence of nutrients on food choice in bamboo-leaf-based macaques is not yet available. Assamese macaques (Macaca assamensis) inhabiting limestone forests are characterized by such a bamboo-leaf-based diet, predominantly consuming young leaves of Bonia saxatilis, a shrubby, karst-endemic bamboo. We studied the feeding behavior of one group of Assamese macaques using instantaneous scan sampling in limestone forests of the Guangxi Nonggang National Nature Reserve in southwest Guangxi, China. We compared the nutrient content of staple food and nonfood items and examine the role of key nutrients in the food selection of macaques. Our results showed that young leaves of bamboo B. saxatilis contained more water, crude protein, phosphorus, and less tannin than nonfood items. Furthermore, staple foods contained a higher content of water and less content of calcium than nonfood items. More specifically, quantities of water, crude protein, calcium, and phosphorus in food items were critical factors affecting feeding time on a specific plant item. Our results suggest that young bamboo leaves could meet macaques' required protein and water intake, while enabling them to maintain their mineral balance, consequently facilitating to maintain the primates' bamboo-leaf-diet in the limestone forest. Our findings confirm the effects of nutrient contents in food choice of Assamese macaques, highlighting the importance of the nutrient contents in maintaining their bamboo-based diet and the need to increase the knowledge on their nutritional strategy adapted to the bamboo-dominated diet inhabiting the unique limestone habitat.
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Data on activity budgets and ranging patterns were collected from March to December 2001 for one group of François' langurs (Trachypithecus francoisi) inhabiting a forested part of the Fusui Nature Reserve, Guangxi province, China. Our results indicate that the total size of the home range of the study group during the study period was 19 ha. The majority of their activities (52%) occurred within a small area, 22%, of their home range, and was concentrated in or near quadrats containing their sleeping sites, which may reduce the time and energetic cost of travel. The extent of the ranging behavior varied between months, with the smallest, 7 ha, recorded in July and the largest, 13.5 ha, in November. There was no significant difference between seasons. The monthly mean daily path lengths varied from 341 to 577 m. The daily path lengths showed significant seasonal changes: the path lengths were longer during the dry season than in the rainy season, which may be related to the scarcity of preferred food resources during the dry season.
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Cercopithecidae/fisiologia , Cercopithecidae/psicologia , Ecossistema , Animais , Animais Selvagens , China , Atividade Motora , Estações do Ano , Sono/fisiologiaRESUMO
Three new troglobitic species of Tomocerus are described from the southwestern karsts of China. All of them have well developed postantennal organs. Tomocerus dong sp. nov. is similar to Tomocerus postantennalis Yu, Zhang & Deharveng and Tomocerus deharvengi sp. nov., but is different from them mainly in the number of prelabral chaetae and the dorsal body chaetotaxy. T. deharvengi sp. nov. is very similar to T. postantennalis but differs from the latter in the cephalic chaetotaxy, the number of manubrial pseudopores and the number of dental spines. T. cthulhu sp. nov. is peculiar for the multi-furcated vesicles of ventral tube, and is different from the three aforementioned species mainly in the dorsal body chaetotaxy. The position of the new species and the relationships between them are discussed.
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Artrópodes/anatomia & histologia , Artrópodes/classificação , Distribuição Animal/fisiologia , Animais , Artrópodes/fisiologia , China , Feminino , Masculino , Especificidade da EspécieRESUMO
Limestone hill habitats pose unique challenges to langurs. One of the characteristics of this habitat is its cliffs, which account for about 10-20% of the total area. We have never observed langurs falling from the cliffs during our 10-year field study. Five patterns of locomotion were exhibited by the white-headed langur: (1) arboreal ascent and descent, (2) arboreal quadupedalism, (3) terrestrial quadrupadelism, (4) moving on cliffs and (5) leaping on cliffs. Locomotor patterns varied according to the substrate, but terrestrial quadrupedalism accounted for more than 50% of locomotion time. Moving on cliffs and leaping on cliffs may be modes of locomotion unique to the white-headed langur, at least in terms of frequency. White-headed langurs have an intermembral index of 76 and, compared to langurs with a similar intermembral index, are more terrestrial. Further analysis indicates that greater terrestrialism may be the result of adaptation to their limestone habitat. Interestingly, white-headed langurs select caves on the cliff as their sleeping sites, and they exhibit special behaviors for exiting and entering the cave very early in the morning and late in the evening.
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Adaptação Biológica/fisiologia , Cercopithecidae/fisiologia , Meio Ambiente , Locomoção/fisiologia , Animais , Pesos e Medidas Corporais , Cercopithecidae/anatomia & histologia , China , Feminino , Estudos Longitudinais , Masculino , Observação , Estatísticas não ParamétricasRESUMO
Two closely related Homidia species, H. fascia Wang & Chen, 2001 and H. pseudofascia sp. nov., are recognized by both morphological and molecular approaches. Both species have minor morphological differences except distinct colour patterns on thorax. Genetic distances (18%) of COI barcodes between them greatly exceed commonly employed threshold (3%), also indicating two independent species. The use of colour pattern in taxonomy of Homidia is also discussed.
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Artrópodes/classificação , Estruturas Animais/anatomia & histologia , Estruturas Animais/crescimento & desenvolvimento , Animais , Artrópodes/anatomia & histologia , Artrópodes/genética , Artrópodes/crescimento & desenvolvimento , Tamanho Corporal , Feminino , Masculino , Tamanho do Órgão , FilogeniaRESUMO
We collected fecal samples of white-headed langurs from 3 of the 4 remaining habitat fragments (Fa, Fb and CZ) located in southwestern Guangxi, China in Nov 2005, and used 5 microsatellite loci and the SRY gene to assess the relatedness between 46 langurs within and between groups. We observed 2 forms of group structure: one-male/multi-female groups (OMGs) and all-male groups (AMGs). One AMG in Fa was composed of 2 generations, included a father, 2 sons and 1 unrelated male, and all OMGs in all 3 habitats included 1 resident male, several adult females and offspring. Of the 21 identified father-offspring cases, the resident male fathered 20 (95%) and the non-resident male sired 1 (5%), suggesting that adult males had overwhelming priority of access to females as the resident male in an OMG, while the non-resident male may also have the opportunity to adopt surreptitious mating strategies.
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Colobinae/genética , Colobinae/fisiologia , Ecossistema , Comportamento Sexual Animal/fisiologia , Comportamento Social , Animais , China , Primers do DNA/genética , Fezes/química , Feminino , Genes sry/genética , Genótipo , Masculino , Repetições de Microssatélites/genética , Reação em Cadeia da Polimerase , Análise para Determinação do Sexo , Fatores SexuaisRESUMO
The large Southeast Asian genus Desmoxytes is slightly rediagnosed. A number of troglomorphic, most likely troglobitic, species occur in southern China. A key is provided to all 10 Desmoxytes spp. currently known from China, including three new presumed troglobites: Desmoxytes eupterygotasp. n. from Hunan Province, as well as Desmoxytes spinissimasp. n. and Desmoxytes luisp. n. from Guangxi Province. "Desmoxytes" philippina Nguyen Duc & Sierwald, 2010, from the Philippines, is formally removed from Desmoxytes, but not assigned to another genus. It probably belongs in a new genus in the subfamily Australiosomatinae, tribe Antichiropodini, close to the Bornean Euphyodesmus Attems, 1931 and Borneochiropus Golovatch, 1996.
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We investigated the diet of a group of François' langur inhabiting a forest fragment between August 2002 and July 2003 to add to our knowledge of behavior and ecology of this langur. Our objective was to study whether the François' langur would adopt a feeding strategy similar to the white-headed langur in the same nature reserve. Data indicated that a total of 37 plant species were eaten by François' langur; however, only ten species accounted for 90% of the total feeding time. Four species belong to the ten most dominant tree species within the vegetation quadrats. Ninety-four percent of feeding time of François' langur was spent on leaves, whereas the remaining 6% of time was spent on fruits, flowers and twigs. Results also demonstrated that François' langur are similar to white-headed langur in being predominantly folivorous and that Francois' langur adopted a similar strategy to white-headed langur in diet, dietary variation and time spent on feeding. François' langur exhibited a habitat use preference for the middle zone of the forest, whereas the white-headed langur utilized the bottom zone of the forest. Further analysis indicates that human interference and habitat fragmentation caused by agriculture also impact habitat use.