Social behaviors of all-male proboscis monkeys when joined by females

In a riverine forest along the Menanggul River, which is a tributary of the Kinabatangan River, Sabah, Malaysia, I observed an all-male group of proboscis monkey (Nasalis larvatus) consisting of 27–30 (mean: 28.8) individuals. This large size of the all-male group seems to be attributed to habitat fragmentation because of the expansion of oil palm plantations. A few females joined this all-male group. Sub-adult females copulated with subadult or large juvenile males. Since the mean male tenure period of this monkey was estimated to be longer than female maturity, and prematured females might leave their natal one-male groups to avoid inbreeding and temporarily participate in the all-male group where males were permissive to them. Even when females joined this group, no conflicts occurred among males.     

Female transfer between one-male groups of proboscis monkey (<Emphasis Type="Italic">Nasalis larvatus</Emphasis>)

Successful or unsuccessful female transfers were observed seven times during a 32-month field study of proboscis monkeys (Nasalis larvatus) inhabiting a riverine forest along a tributary of the Kinabatangan River, Sabah, Malaysia. In all cases, the females voluntarily left their own groups and immediately joined with another one. When adult females tried to shift to other groups, adult males called them back to their own groups, but appeared to be indifferent to subadult females. When the adult females returned, the males never attacked the females physically, but instead often emitted herding sounds to them. One subadult female was repelled by a resident adult female. When one adult female transferred into a new one-male group, she left her behind son in an all-male group. The number of females often fluctuated in most study groups, with this fluctuation being more prominent among subadult females than adult females. It is likely that female transfer in proboscis monkeys is not a rare occurrence and that it is especially common among sub-adult females.     

Ecology and behavior of the wild proboscis monkey,Nasalis larvatus (Wurmb), in Sabah,Malaysia

Proboscis monkeys,Nasalis larvatus (Wurmb), were investigated in the Padas Bay and Kinabatangan River areas, Sabah, from July 1968 to March 1969. The proboscis monkey is a common, widely distributed species of coloboids in Sabah, living in the various vegetations that extend from the coastal swamp to the inland plain. It appears to have a terrestrial tendency, compared with other coloboids, moving around on the ground in the forest and extending its activity, sometimes, to the open land along the river beach. The number of monkey in a troop, we observed, ranged from 11 to 32, and almost all troops were composed of several adult males, many more adult females, and immature animals. The adult males appear to play the role of leaders in the troop through their characteristic behavior, attacking, threatening, warning, watching, etc., other troop members or invaders. Each troop always emitted various boisterous vocalizations which were divided into 14 types.     

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Proboscis monkeys' (Nasalis larvatus) river crossing behavior was examined as a potential behavioral response to predation threat. N. larvatus' major predator at the Tanjung Puting National Park in Kalimantan Tengah, Indonesia, appeared to be the false gavial (Tomistoma schlegeli), a crocodilian. An adolescent female proboscis monkey was captured and drowned by a false gavial during this study. The monkeys crossed the river at its more narrow points, with several individuals or groups crossing simultaneously. Increased vigilance prior to crossing and leaping as far across the river as possible were also observed. Proboscis monkey groups often associate at their sleeping sites at the river's edge. A potential function of these associations may be to allow groups to synchronize their movement with other groups during river crossings.     

Feeding ecology of the proboscis monkey (Nasalis larvatus)

Proboscis monkey (Nasalis larvatus) feeding behavior and ecology were studied at the Natai Lengkuas Station, Tanjung Puting National Park, Kalimantan Tengah, Indonesia. Data on feeding behavior were collected using scan sampling during group follows. Three vegetational plots containing 1,732 trees were established and monitored monthly for changes in fruit, flower, and young leaf production. Basal area and canopy cover were calculated and used in estimating food abundance. Proboscis monkeys were found to be folivore/frugivores, specializing in seed consumption. At least 55 different plant species were used as food sources, with a marked preference for Eugenia sp. 3/4,Ganua motleyana and Lophopetalum javanicum. These tree species were among the most frequent and most dominant. However, proboscis monkeys were selective feeders; use of tree species as food sources was not based simply on relative density. During times of low food abundance and/or availability proboscis monkeys switched dietary strategies and increased dietary diversity. The average total home range was estimated to be 130.3 ha, with an average group density of 5.2 groups per km². The average biomass per km² was estimated to be 499.5 kg. Given their high biomass and predilection for consuming seeds of dominant species, proboscis monkeys may help to maintain and increase vegetational diversity.     

Does intraspecific variation in social systems explain reported differences in the social structure of the proboscis monkey (Nasalis larvatus)?

The social structure of proboscis monkeys (Nasalis larvatus) was investigated in the Brunei Bay area of Brunei Darussalam (Northern Borneo). Intraspecific variability in social systems had been suggested to occur in this species, with social structure varying with habitat differences. Prior reports for this area suggested that groups contained several males, females, and offspring and were unstable. Contrary to these reports, I found that the monkeys were organized into groups containing one male, several females, and offspring. These groups associated at sleeping sites at the river’s edge, thus forming a secondary level of organization. This is the same social system reported in Sarawak, Malaysia and Kalimantan, Indonesia in different habitat types. It appears that methodological differences may account for the discrepancies between reports. I have found no evidence to suggest that intraspecific variation in social systems occurs in this species.     

Crocodile predation on a proboscis monkey in Borneo

An adult male proboscis monkey (Nasalis larvatus) on the edge of the Sekonyer Kanan River was seized by a crocodile 6 km downstream from the Orangutan Research and Conservation Project base camp where a crocodile had taken a crab-eating macaque (Macaca fascicularis) two years earlier. This incident helps establish false gavials (Tomistoma schlegeli) as important predators on refuging primate populations in southern Borneo and indicates that predation may have influenced the evolution of some behaviors with an antipredator function in bothNasalis andMacaca fascicularis.     

Feed intake,digestion and passage of the proboscis monkey (Nasalis larvatus) in captivity

Feeding trials were conducted with a troop of six proboscis monkeys (Nasalis larvatus) at the New York Zoological Park to quantify aspects of digestive physiology. Diets consumed comprised, on an as-fed basis, 55% browse and green produce, 11% fruit, 9% commercial primate diets, 9% root vegetables, and 16% miscellaneous items. Total feed intake averaged 12% of body mass; dry matter intake was 3%. Dry matter and plant cell wall disappearance exceeded 80%. Passage marker studies (three 6-day trials) revealed: transit time=14 hr; mean passage time=49 hr; and 5–80% retention time=52 hr. Digestion coefficients and retention times were greater than expected based on body size. These results might reflect the low fiber content of the diets fed, or alternatively, provide evidence that proboscis monkeys are efficient digesters of cell wall constituents.     

Ranging Behavior of Proboscis Monkeys in a Riverine Forest with Special Reference to Ranging in Inland Forest

We observed a unimale group (BE-Group) of proboscis monkeys (Nasalis larvatus) comprising an α-male, 6 adult females, and several immatures from May 2005 to May 2006. We followed the group for 2014 h along the Menanggul River, Sabah, Malaysia (118°30′E, 5°30′N). Observations focused mainly on ranging behavior. We determined availability and seasonal changes in plant species consumed by the members of the group by vegetation surveys in a 2.15-ha area along 200–500 m trails in the riverine forest. During the observation period, the group ranged ≤800 m from the riverbank, within a total range of 138.3 ha. The daily path length of the group ranged from 220 to 1734 m (mean, 799 m), and daily path length correlates negatively with fruit availability. The monkeys were apt to remain within a small range in fruit-abundant seasons. Because the monkeys preferred to feed on fruits of dominant plant species in the study area, their daily path length may decrease on days when they feed on fruits. The core areas of the group’s home range were along the river because the monkeys typically returned to riverside trees to sleep. The group most often used areas that were nearer the riverbank and where the availability of fruits was higher. The most frequently used grids were the ones where the group often had sleeping sites and crossed the river. Avoiding predation may be the main reason for river crossing and selecting particular sleeping sites; hence not only food availability but also the risk of predation appears to influence the ranging of the BE-Group.     

Daily feeding rhythm in proboscis monkeys: a preliminary comparison with other non-human primates

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.     

Metric and morphological variability in the dentition of Colobine monkeys

A morphological study was performed using 97 Colobus polykomos and 41 Nasalis larvatus. The premolars and molars of these two taxa of leaf-eating monkeys were similar in that they possessed deeply grooved and highly pointed cusps. Of 7 dental traits investigated, 4 were significantly different between the 2 forms. Indeed, with 2 of these, the position of the lingual cusp on PM₄ and the number of cusps on PM³ displayed highly contrasting structures.Metric analysis was conducted using 47 C. polykomos and 37 N. larvatus specimens. Mesiodistal and buccolingual measurements were taken on the upper canine and all postcanine teeth. Sexual dimorphism was detected in most maxillary dental measurements and all mandibular estimates of both species. In all cases, males exceeded females in tooth diameter. Testing between species by sex revealed that C. polykomos was significantly larger in several canine and premolar dimensions while N. larvatus had significantly larger molar dimensions. An additional 73 measurements were selected to represent occluding dental structures and a morphological integration analysis was conducted. Results of this analysis indicated that C. polykomos possessed a C¹-PM₃ complex which was more highly intercorrelated whereas the broad lophed N. larvatus molars constituted a more highly correlated functional unit.It was suggested that the above differences between these two groups of leaf-eating monkeys probably resulted from inbreeding, isolation and drift.     

Proboscis monkey (Nasalis larvatus) social organization: Group structure

Proboscis monkey (Nasalis larvatus) social organization was studied at the Tanjung Puting National Park in Kalimantan Tengah, Indonesia, for 12 months. Data were collected on one-male groups and all-male groups by using scan sampling and event sampling while following groups. Evening census surveys were also conducted. Proboscis monkeys were found to follow the typical Asian colobine pattern of one-male social groups, with extra-group males forming all-male groups. These groups appear stable, with few changes in membership. One-male groups appear to be “female bonded”; adult females direct affiliative behaviors towards their offspring and other adult females, not towards the male. Nearest-neighbor data indicate some peripheralization of juvenile animals.     

Multiple Ecological Factors Influence the Location of Proboscis Monkey (<Emphasis Type="Italic">Nasalis larvatus</Emphasis>) Sleeping Sites in West Kalimantan,Indonesia

Multiple ecological factors have been hypothesized to influence primate sleeping site selection. Testing multiple hypotheses about sleeping site selection permits examination of the relative strength of distinct ecological factors and expands our ability to understand how selection pressures influence primate sleeping behavior. Here we examine how avoidance of biting insects, thermoregulation, foraging efficiency, tree stability, and interspecific competition influence selection of sleeping sites by proboscis monkeys (Nasalis larvatus) in Indonesian Borneo. We collected data on relative insect abundance, temperature, rainfall, food availability, group size, sleeping site location, and presence of other primates for 12 mo. Using formal model comparison and information criteria, we analyzed the relative importance of these ecological factors in determining one aspect of sleeping site location: distance from the river. Our models supported the avoidance of biting insects and the foraging efficiency hypotheses. Proboscis monkeys slept further inland on nights when the abundance of sandflies was high along the river, and when less food was available along the river. Many studies suggest that primates select sleeping trees and locations to reduce predation risk; our study indicates that additional factors may also be important in determining sleeping site selection.     

Proboscis monkey (Nasalis larvatus) social organization: Nature and possible functions of intergroup patterns of association

Proboscis monkey (Nasalis larvatus) socioecology was studied at the Natai Lengkuas Station, Tanjung Puting National Park, in Kalimantan Tengah, Indonesia. Data on the nature of intergroup interactions were collected on ten one-male groups and two all-male groups using event sampling during follows and also through evening census surveys. Proboscis monkeys form stable one-male groups, with specific groups regularly associating at their sleeping sites (band members). Both intraband and interband high-intensity agonistic displays (slapping, chasing, biting) were rare. Lower intensity agonistic displays (vocalizations, leaping-branch shaking, and erect penis and open-mouth displays) occurred frequently. Temporal avoidance between bands may have been mediated by early morning vocalizations and branch shaking displays by the adult males. Associations between groups may play a role in displacement avoidance and/or predation avoidance.     

The ontogeny of cranial sexual dimorphism in two old world monkeys:Macaca fascicularis (Cercopithecinae) andNasalis larvatus (Colobinae)

Allometric and heterochronic approaches to sexual dimorphism have contributed much to our understanding of the evolutionary morphology of the primate skull and dentition. To date, however, extensive studies of sexual dimorphism have been carried out only on the great apes and a few cercopithecine monkeys. To fill this gap, representative dimensions of the skull were collected among ontogenetic series of two dimorphic Old World monkeys:Macaca fascicularis (Cercopithecinae) andNasalis larvatus (Colobinae). The ontogeny of cranial sexual dimorphism was evaluated with least-squares bivariate regression, analysis of covariance (ANCOVA), and analysis of variance (ANOVA). Results indicate that within each species the sexes typically exhibit nonsignificant differences in ANCOVAs of ontogenetic trajectories, except for bivariate comparisons with bicanine breadth. AmongMacaca fascicularis, ANOVAs between males and females of common dental ages show that adult, and frequently subadult, males are significantly larger than females, i.e., sexual dimorphism develops via time and rate hypermorphosis (males primarily grow for a longer time period as well as faster). AmongNasalis larvatus, however, comparisons between males and females of common dental ages indicate that only adult males are significantly larger than females, i.e., sexual dimorphism develops primarily via time hypermorphosis (males grow for a longer time period). Within both species, females appear to exhibit an early growth spurt at dental age 2; that is, many cranial measures for females tend to be larger than those for males. Measures of the circumorbital region (e.g., browridge height), body weight, and bicanine breadth exhibit typically the highest sexual dimorphism ratios. The fact that postcanine toothrow length and neurocranial volume (less so inNasalis) demonstrate very low dimorphism ratios generally supports assertions that postnatal systemic growth (and associated selective pressures thereon) exerts a greater influence on facial, but not neural, dental, or orbital, development (Cochard, 1985, 1987; Shea, 1985a,b, 1986; Shea and Gomez, 1988; Sheaet al., 1990). Additional consideration of ontogenetic differences between species generally supports previous functional interpretations of subfamilial differences in cranial form related to agonistic displays in cercopithecine monkeys (Ravosa, 1990).     

Feeding and ranging in the Mentawai Island langur (Presbytis potenziani)

Presbytis potenziani is found only on the Mentawai Islands, Indonesia, and its ecology and feeding and ranging behavior have been little studied. I studied 10 groups ofPresbytis potenziani in the primary forests of North Pagai Island, Mentawai, Indonesia.P. potenziani used primarily the upper strata of the forests for feeding, movement, and resting. Groups remained cohesive during their daily activities, ranged between 100 to > 1000 m daily, and occupied home ranges of ≤ 40 ha. Neither sex predominantly initiated group movement. Locomotion was primarily quadrupedal, with frequent leaping. P. potenziani showed two feeding peaks, one in early morning and one during midafternoon. P. potenziani fed mainly on climbers and trees of the Dipterocarpaceae. They ate primarily leaves, but also fed on fruits and other plant parts.     

A 2.6 kb intron separates the signal peptide coding sequence of an anther-specific protein from the rest of the gene in sunflower

Summary Metabolism of sulfonylurea herbicides by Streptomyces griseolus ATCC 11796 is carried out via two cytochromes P-450, P-450_SU1 and P-450_SU2. Mutants of S. griseolus, selected by their reduced ability to metabolize a fluorescent sulfonylurea, do not synthesize cytochrome P-450_SU1 when grown in the presence of sulfonylureas. Genetic evidence indicated that this phenotype was the result of a deletion of > 15 kb of DNA, including the structural genes for cytochrome P-450_SU1 and an associated ferredoxin Fd-1 (suaC and suaB, respectively). In the absence of this monooxygenase system, the mutants described here respond to the presence of sulfonylureas or phenobarbital in the growth medium with the expression of only the suhC,B gene products (cytochrome P-450_SU2 and Fd-2), previously observed only as minor components in wild-type cells treated with sulfonylurea. These strains have enabled an analysis of sulfonylurea metabolism mediated by cytochrome P-450_SU2 in the absence of P-450_SU1, yielding an in vivo delineation of the roles of the two different cytochrome P-450 systems in herbicide metabolism by S. griseolus.     

Clouded leopard (<Emphasis Type="Italic">Neofelis diardi</Emphasis>) predation on proboscis monkeys (<Emphasis Type="Italic">Nasalis larvatus</Emphasis>) in Sabah,Malaysia

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.     

In vivo analysis of <Emphasis Type="Italic">Drosophila</Emphasis> SU(<Emphasis Type="Italic">Z</Emphasis>)12 function

Polycomb group (PcG) proteins are required to maintain a stable repression of the homeotic genes during Drosophila development. Mutants in the PcG gene Supressor of zeste 12 (Su(z)12) exhibit strong homeotic transformations caused by widespread misexpression of several homeotic genes in embryos and larvae. Su(z)12 has also been suggested to be involved in position effect variegation and in regulation of the white gene expression in combination with zeste. To elucidate whether SU(Z)12 has any such direct functions we investigated the binding pattern to polytene chromosomes and compared the localization to other proteins. We found that SU(Z)12 binds to about 90 specific eukaryotic sites, however, not the white locus. We also find staining at the chromocenter and the nucleolus. The binding along chromosome arms is mostly in interbands and these sites correlate precisely with those of Enhancer-of-zeste and other components of the PRC2 silencing complex. This implies that SU(Z)12 mainly exists in complex with PRC2. Comparisons with other PcG protein-binding patterns reveal extensive overlap. However, SU(Z)12 binding sites and histone 3 trimethylated lysine 27 residues (3meK27 H3) do not correlate that well. Still, we show that Su(z)12 is essential for tri-methylation of the lysine 27 residue of histone H3 in vivo, and that overexpression of SU(Z)12 in somatic clones results in higher levels of histone methylation, indicating that SU(Z)12 is rate limiting for the enzymatic activity of PRC2. In addition, we analyzed the binding pattern of Heterochromatin Protein 1 (HP1) and found that SU(Z)12 and HP1 do not co-localize.     

Proboscis monkey (Nasalis larvatus) social organization: Intergroup patterns of association

Proboscis monkey (Nasalis larvatus) social organization was studied at the Natai Lengkuas station, Tanjung Puting National Park in Kalimantan Tengah, Indonesia. Data were collected on ten one-male groups and two all-male groups using scan sampling and event sampling during follows, and through evening census surveys. Proboscis monkeys were found to form stable one-male groups. Specific groups associated at their sleeping sites, in a manner similar to the fission-fusion pattern described for hamadryas and gelada baboons. Analyses performed on these associations indicated that the groups formed two separate bands. These separate bands appear to be a secondary level of organization, distinct from the primary level of organization, the one-male and all-male groups. This is the first evidence for such a two-tiered system of organization in an arboreal colobine species. Proboscis monkeys closely resemble gelada baboons in their organizational pattern. In both species, adult females direct the majority of their affiliative behavior towards their offspring and other adult females, males do not engage in active herding, all-male groups are present, and one-male groups do spend time apart from other groups. Home ranges of both groups and of bands of proboscis monkeys overlapped extensively; temporal avoidance between bands may have been mediated by early morning vocalizations and branch shaking displays.