Displaying all 13 publications

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  1. Matsuda I, Tuuga A, Bernard H, Furuichi T
    Primates, 2012 Jan;53(1):13-23.
    PMID: 21773757 DOI: 10.1007/s10329-011-0259-1
    This is the first report on inter-individual relationships within a one-male group of proboscis monkeys (Nasalis larvatus) based on detailed identification of individuals. From May 2005 to 2006, focal and ad libitum data of agonistic and grooming behaviour were collected in a forest along the Menanggul River, Sabah, Malaysia. During the study period, we collected over 1,968 h of focal data on the adult male and 1,539 h of focal data on the six females. Their social interactions, including agonistic and grooming behaviour, appeared to follow typical patterns reported for other colobines: the incidence of social interaction within groups is low. Of 39 agonistic events, 26 were displacement from sleeping places along the river, 6 were the α male threatening other monkeys to mediate quarrels between females and between females and juveniles, and 7 were displacement from feeding places. Although the agonistic behaviour matrix based on the 33 intra-group agonistic events (excluding events between adults and juveniles and between adults and infants) was indicative of non-significant linearity, there were some specific dominated individuals within the group of proboscis monkeys. Nonetheless, grooming behaviour among adult females within a group were not affected by the dominance hierarchy. This study also conducted initial comparisons of grooming patterns among proboscis monkeys and other primate species. On the basis of comparison of their grooming networks, similar grooming patterns among both-sex-disperse and male-philopatric/female-disperse species were detected. Because adult females in these species migrate to groups repeatedly, it may be difficult to establish the firm grooming exchange relationship for particular individuals within groups, unlike in female-philopatric/male-disperse species. However, grooming distribution patterns within groups among primate species were difficult to explain solely on the basis of their dispersal patterns. Newly immigrated females in some species including proboscis monkeys are eager to have social interactions with senior group members to improve their social position.
  2. Matsuda I, Kubo T, Tuuga A, Higashi S
    Am. J. Phys. Anthropol., 2010 Jun;142(2):235-45.
    PMID: 20091847 DOI: 10.1002/ajpa.21218
    To understand the effects of environmental factors on a social system with multilevel society in proboscis monkey units, the temporal change of the local density of sleeping sites of monkeys was investigated along the Menanggul river from May 2005 to 2006 in Malaysia. Proboscis monkeys typically return to riverside trees for night sleeping. The sleeping site locations of a one-male unit (BE-unit) were recorded and the locations of other one-male and all-male units within 500 m of the BE-unit were verified. In addition, environmental factors (food availability, the water level of the river, and the river width) and copulation frequency of BE-unit were recorded. From the analyses of the distance from the BE-unit to the nearest neighbor unit, no spatial clumping of the sleeping sites of monkey units on a smaller scale was detected. The results of a Bayesian analysis suggest that the conditional local density around the BE-unit can be predicted by the spatial heterogeneity along the river and by the temporal change of food availability, that is, the local density of monkey units might increase due to better sleeping sites with regard to predator attacks and clumped food sources; proboscis monkeys might not exhibit high-level social organization previously reported. In addition, this study shows the importance of data analysis that considers the effects of temporal autocorrelation, because the daily measurements of longitudinal data on monkeys are not independent of each other.
  3. Matsuda I, Tuuga A, Higashi S
    Am. J. Primatol., 2009 Jun;71(6):478-92.
    PMID: 19288553 DOI: 10.1002/ajp.20677
    A group of proboscis monkeys (Nasalis larvatus) consisting of an alpha-male, six adult females, and several immatures was observed from May 2005-2006. We collected over 1,968 hr of focal data on the adult male and 1,539 hr of focal data on the six females in a forest along the Menanggul River, Sabah, Malaysia. Availability and seasonal changes in plant species consumed by the focal monkeys were determined by vegetation surveys carried out across an area of 2.15 ha along 200-500 m trails in riverine forest. A total of 188 plant species were consumed by the focal monkeys. The activity budget of members of our study group was 76.5% resting, 19.5% feeding, and 3.5% moving. Young leaves (65.9%) and fruits (25.9%) accounted for the majority of feeding time. Over 90% of fruit feeding involved the consumption of unripe fruits and in the majority of case both the fruit flesh and seeds were eaten. Although fruit eating was rare in some months, during other times of the year time fruit feeding exceeded the time devoted to young leaves. We found that monthly fruit availability was positively related to monthly fruit eating and feeding activity, and seasonal fluctuations in dietary diversity were significantly affected by fruit eating. These results suggest that fruit availability and fruit-eating behaviors are key factors that influence the activity budget of proboscis monkeys. Earlier assumptions that colobine monkeys are obligate folivores do not apply well to proboscis monkeys and certain other colobines. Our findings may help contribute to a better understanding of the dietary adaptations and feeding ecology of Asian colobines.
  4. Matsuda I, Tuuga A, Higashi S
    Primates, 2008 Jul;49(3):227-31.
    PMID: 18484152 DOI: 10.1007/s10329-008-0085-2
    In this study, we have reported two direct observations of individuals from a one-male group of proboscis monkeys (Nasalis larvatus) being killed by clouded leopards (Neofelis diardi) in the riverine forest along the Menanggul river, a tributary of the Kinabatangan river in Sabah, Malaysia. One of the two individuals was an infant female and the other was a juvenile female. Based on literature reviews and the observations reported here, we suggest that clouded leopard and crocodile might be significant potential predators of proboscis monkeys of any age or sex and that predation threats elicit the monkeys' anti-predator strategies. Moreover, the observations of the monkeys' behaviour when the group is attacked by a predator suggest that the adult males in one-male groups play an important role as protectors.
  5. Matsuda I, Tuuga A, Akiyama Y, Higashi S
    Am. J. Primatol., 2008 Nov;70(11):1097-101.
    PMID: 18651612 DOI: 10.1002/ajp.20604
    From May 2005-2006, selections of river crossing locations and sleeping sites used by a one-male group (BE-Group) of proboscis monkeys (Nasalis larvatus) were investigated along the Menanggul River, tributary of the Kinabatangan River, Sabah, Malaysia. The frequency of river crossings for focal monkeys in the BE-Group was significantly higher at locations with narrow branch-to-bank distances. Branch-to-bank distances were defined as the distances between the longest tree branches extending over the river and the bank of river on each side. This was measured in areas crossed by the monkeys. The focal monkeys used locations with a higher probability of successful river crossings that did not require jumping into the water and swimming across than those that did. The frequency of sleeping site usage by the BE-Group was positively correlated with the frequency of using river crossing locations by the focal monkeys. Previous reports on predation of proboscis monkeys indicate that clouded leopards (Neofelis diardi) and crocodilians (Tomistoma schlegeli and Crocodylus porosus) may be the major terrestrial and aquatic predators of these monkeys. The selection of river crossing locations by proboscis monkeys may be influenced both by the threat of these predators and the location of suitable and protected sleeping sites. Finally, sleeping sites locations that offer arboreal escape routes may protect proboscis monkeys from leopard attack.
  6. Matsuda I, Akiyama Y, Tuuga A, Bernard H, Clauss M
    Primates, 2014 Apr;55(2):313-26.
    PMID: 24504856 DOI: 10.1007/s10329-014-0407-5
    In non-human primates, the daily feeding rhythm, i.e., temporal fluctuation in feeding activity across the day, has been described but has rarely received much analytical interpretation, though it may play a crucial part in understanding the adaptive significance of primate foraging strategies. This study is the first to describe the detailed daily feeding rhythm in proboscis monkeys (Nasalis larvatus) based on data collected from both riverbank and inland habitats. From May 2005 to May 2006, data on feeding behavior in a group of proboscis monkeys consisting of an alpha-male, six adult females and immatures was collected via continuous focal animal sampling technique in a forest along the Menanggul River, Sabah, Malaysia. In both the male and females, the highest peak of feeding activity was in the late afternoon at 15:00-17:00, i.e., shortly before sleeping. The differences in the feeding rhythm among the seasons appeared to reflect the time spent eating fruit and/or the availability of fruit; clearer feeding peaks were detected when the monkeys spent a relevant amount of time eating fruit, but no clear peak was detected when fruit eating was less frequent. The daily feeding rhythm was not strongly influenced by daily temperature fluctuations. When comparing the daily feeding rhythm of proboscis monkeys to that of other primates, one of the most common temporal patterns detected across primates was a feeding peak in the late afternoon, although it was impossible to demonstrate this statistically because of methodological differences among studies.
  7. Matsuda I, Higashi S, Otani Y, Tuuga A, Bernard H, Corlett RT
    Integr Zool, 2013 Dec;8(4):395-9.
    PMID: 24344963 DOI: 10.1111/1749-4877.12033
    Although the role of primates in seed dispersal is generally well recognized, this is not the case for colobines, which are widely distributed in Asian and African tropical forests. Colobines consume leaves, seeds and fruits, usually unripe. A group of proboscis monkeys (Colobinae, Nasalis larvatus) consisting of 1 alpha-male, 6 adult females and several immatures, was observed from May 2005 to May 2006. A total of 400 fecal samples from focal group members covering 13 months were examined, with over 3500 h of focal observation data on the group members in a forest along the Menanggul River, Sabah, Malaysia. Intact small seeds were only found in 23 of 71 samples in Nov 2005, 15 of 38 in Dec 2005 and 5 of 21 in Mar 2006. Seeds of Ficus (all <1.5 mm in length) were found in all 3 months and seeds from Antidesma thwaitesianum (all <3 mm) and Nauclea subdita (all <2 mm) only in Nov and Dec, which was consistent with members of the study group consuming fruits of these species mostly at these times. To our knowledge, these are the first records of seeds in the fecal samples of colobines. Even if colobines pass relatively few seeds intact, their high abundance and biomass could make them quantitatively significant in seed dispersal. The potential role of colobines as seed dispersers should be considered by colobine researchers.
  8. Matsuda I, Clauss M, Tuuga A, Sugau J, Hanya G, Yumoto T, et al.
    Sci Rep, 2017 02 17;7:42774.
    PMID: 28211530 DOI: 10.1038/srep42774
    Free-living animals must make dietary choices in terms of chemical and physical properties, depending on their digestive physiology and availability of food resources. Here we comprehensively evaluated the dietary choices of proboscis monkeys (Nasalis larvatus) consuming young leaves. We analysed the data for leaf toughness and digestibility measured by an in vitro gas production method, in addition to previously reported data on nutrient composition. Leaf toughness, in general, negatively correlated with the crude protein content, one of the most important nutritional factors affecting food selection by leaf-eating primates. This result suggests that leaf toughness assessed by oral sensation might be a proximate cue for its protein content. We confirmed the importance of the leaf chemical properties in terms of preference shown by N. larvatus; leaves with high protein content and low neutral detergent fibre levels were preferred to those of the common plant species. We also found that these preferred leaves were less tough and more digestible than the alternatives. Our in vitro results also suggested that N. larvatus were little affected by secondary plant compounds. However, the spatial distribution pattern of plant species was the strongest factor explaining the selection of the preferred leaf species.
  9. Ancrenaz M, Gimenez O, Ambu L, Ancrenaz K, Andau P, Goossens B, et al.
    PLoS Biol., 2005 Jan;3(1):e3.
    PMID: 15630475
    Great apes are threatened with extinction, but precise information about the distribution and size of most populations is currently lacking. We conducted orangutan nest counts in the Malaysian state of Sabah (North Borneo), using a combination of ground and helicopter surveys, and provided a way to estimate the current distribution and size of the populations living throughout the entire state. We show that the number of nests detected during aerial surveys is directly related to the estimated true animal density and that a helicopter is an efficient tool to provide robust estimates of orangutan numbers. Our results reveal that with a total estimated population size of about 11,000 individuals, Sabah is one of the main strongholds for orangutans in North Borneo. More than 60% of orangutans living in the state occur outside protected areas, in production forests that have been through several rounds of logging extraction and are still exploited for timber. The role of exploited forests clearly merits further investigation for orangutan conservation in Sabah.
  10. Koda H, Murai T, Tuuga A, Goossens B, Nathan SKSS, Stark DJ, et al.
    Sci Adv, 2018 02;4(2):eaaq0250.
    PMID: 29507881 DOI: 10.1126/sciadv.aaq0250
    Male proboscis monkeys have uniquely enlarged noses that are prominent adornments, which may have evolved through their sexually competitive harem group social system. Nevertheless, the ecological roles of the signals encoded by enlarged noses remain unclear. We found significant correlations among nose, body, and testis sizes and a clear link between nose size and number of harem females. Therefore, there is evidence supporting both male-male competition and female choice as causal factors in the evolution of enlarged male noses. We also observed that nasal enlargement systematically modifies the resonance properties of male vocalizations, which probably encode male quality. Our results indicate that the audiovisual contributions of enlarged male noses serve as advertisements to females in their mate selection. This is the first primate research to evaluate the evolutionary processes involved in linking morphology, acoustics, and socioecology with unique masculine characteristics.
  11. Matsuda I, Bernard H, Tuuga A, Nathan SKSS, Sha JCM, Osman I, et al.
    Front Vet Sci, 2017;4:246.
    PMID: 29404345 DOI: 10.3389/fvets.2017.00246
    Understanding the natural diet of species may provide useful information that can contribute to successful captive maintenance. A common problem experienced with captive foregut-fermenting primate (colobine) diets is that they are deficient in fiber and therefore highly digestible. This may contribute to gastrointestinal disorders often observed in zoos. An approach to obtain information relevant for the improvement of diets is to compare the nutrient composition of feces from free-ranging and captive individuals. In theory, fecal material can be considered a proxy for diet intake integrated over a certain period of time. We collected fecal samples from eight free-ranging proboscis monkey (Nasalis larvatus, a highly endangered colobine species) groups from a secondary forest along the Kinabatangan River and four from a mixed mangrove-riverine forest along the Garama River, Sabah, Borneo, Malaysia. We also collected fecal samples from 12 individual captive adult/sub-adult proboscis monkeys from three different zoos. We confirmed that feces from free-ranging monkeys contained more fiber and less metabolic fecal nitrogen than those from captive specimens, indicating a less digestible diet in the wild. Modifying the diets of captive colobines to include more fiber, comparable to those of free-ranging ones, may contribute to their health and survival.
  12. Hayakawa T, Nathan SKSS, Stark DJ, Saldivar DAR, Sipangkui R, Goossens B, et al.
    Environ Microbiol Rep, 2018 12;10(6):655-662.
    PMID: 29992728 DOI: 10.1111/1758-2229.12677
    Foregut fermentation is well known to occur in a wide range of mammalian species and in a single bird species. Yet, the foregut microbial community of free-ranging, foregut-fermenting monkeys, that is, colobines, has not been investigated so far. We analysed the foregut microbiomes in four free-ranging proboscis monkeys (Nasalis larvatus) from two different tropical habitats with varying plant diversity (mangrove and riverine forests), in an individual from a semi-free-ranging setting with supplemental feeding, and in an individual from captivity, using high-throughput sequencing based on 16S ribosomal RNA genes. We found a decrease in foregut microbial diversity from a diverse natural habitat (riverine forest) to a low diverse natural habitat (mangrove forest), to human-related environments. Of a total of 2700 bacterial operational taxonomic units (OTUs) detected in all environments, only 153 OTUs were shared across all individuals, suggesting that they were not influenced by diet or habitat. These OTUs were dominated by Firmicutes and Proteobacteria. The relative abundance of the habitat-specific microbial communities showed a wide range of differences among living environments, although such bacterial communities appeared to be dominated by Firmicutes and Bacteroidetes, suggesting that those phyla are key to understanding the adaptive strategy in proboscis monkeys living in different habitats.
  13. Nater A, Mattle-Greminger MP, Nurcahyo A, Nowak MG, de Manuel M, Desai T, et al.
    Curr. Biol., 2017 Nov 20;27(22):3487-3498.e10.
    PMID: 29103940 DOI: 10.1016/j.cub.2017.09.047
    Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.
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