Ikki Matsuda

Multilevel Societies in Primates and Other Mammals: Introduction to the Special Issue.

Murdoch (1981) remarked that nowhere on Earth do people live regularly in isolated families. The habitual formation of superfamily level groupings is one of the unmistakable universals of human sociality. Males and females within these higher level groupings are connected via kinship and affinity ties, and affiliative and cooperative bonds reach far beyond the nuclear family unit (Rodseth et al. 1991; Wiessner 1977). Although interunit encounters are usually circumvented or characterized by animosity because of mating or resource competition in many nonhuman primates (Cheney 1987; Fashing 2001), some primates such as hamadryas baboons (Papio hamadryas), geladas (Theropithecus gelada), snub-nosed monkeys (Rhinopithecus spp.), and proboscis monkeys (Nasalis larvatus) (for an exhaustive list, see Grueter et al. 2012) exhibit a social arrangement in which regular or constant proximity as well as coordinated activity among subunits is the norm. This type of social organization has been termed multilevel, nested, or modular. The phenomenon of social modularity is not restricted to the primate order. Similarly structured societies can be observed in other mammals, most notably African elephants (Loxodonta africana: de Silva and Wittemyer 2012; Moss and Poole 1983; Wittemyer et al. 2005), Asian elephants (Elephas maximus: de Silva and Wittemyer 2012), plains zebras (Equus burchelli: Rubenstein and Hack 2004), khulans (Equus hemionus: Feh et al. 2001), prairie dogs (Cynomys ludovicianus: Hoogland 1995), sperm whales (Physeter macrocephalus: Whitehead et al. 1991, 2012), and killer whales (Orcinus orca: Baird 2000).

Coming down from the trees: Is terrestrial activity in Bornean orangutans natural or disturbance driven?

The orangutan is the worlds largest arboreal mammal, and images of the red ape moving through the tropical forest canopy symbolise its typical arboreal behaviour. Records of terrestrial behaviour are scarce and often associated with habitat disturbance. We conducted a large-scale species-level analysis of ground-based camera-trapping data to evaluate the extent to which Bornean orangutans Pongo pygmaeus come down from the trees to travel terrestrially, and whether they are indeed forced to the ground primarily by anthropogenic forest disturbances. Although the degree of forest disturbance and canopy gap size influenced terrestriality, orangutans were recorded on the ground as frequently in heavily degraded habitats as in primary forests. Furthermore, all age-sex classes were recorded on the ground (flanged males more often). This suggests that terrestrial locomotion is part of the Bornean orangutans natural behavioural repertoire to a much greater extent than previously thought, and is only modified by habitat disturbance. The capacity of orangutans to come down from the trees may increase their ability to cope with at least smaller-scale forest fragmentation, and to cross moderately open spaces in mosaic landscapes, although the extent of this versatility remains to be investigated.

Comparisons of Intraunit Relationships in Nonhuman Primates Living in Multilevel Social Systems

Multilevel social systems have evolved in several species of cercopithecoid primates and appear to be an effective means of changing group size amid variation in environmental conditions. Larger groupings of these species fission and fuse, making intraunit relationships essential to maintain the integrity of the smallest social units. We examine these intraunit relationships in four primates with multilevel social systems: proboscis monkeys (Nasalis larvatus), snub-nosed monkeys (Rhinopithecus roxellana), hamadryas baboons (Papio hamadryas), and geladas (Theropithecus gelada), using social network analysis. The proboscis monkeys and hamadryas baboons were wild and unprovisioned, whereas the snub-nosed monkeys and geladas were partly provisioned. Comparison of eigenvector centrality coefficients revealed a phylogenetic difference in the key individuals maintaining social networks between the colobines and the cercopithecines: females were more central in proboscis and snub-nosed monkeys, with males generally peripheral to social interaction, whereas males were more central than females in geladas and hamadryas. A comparison of sex differences in clustering coefficients, however, revealed a significant difference only in geladas, suggesting that one-male–multifemale units in this species become more unstable when females, but not males, are removed from social networks. Taken together, our results reveal the strongest differences between geladas, characterized by female philopatry and male dispersal, and the three species with bisexual dispersal. These results demonstrate the potential for social network analysis to reveal the social bonds most important for maintaining cohesion of the smallest units of primate multilevel societies. This, in turn, can serve as a proxy, in the absence of long-term data, for underlying patterns of sex-biased dispersal and philopatry.

Leaf Selection by Two Bornean Colobine Monkeys in Relation to Plant Chemistry and Abundance

Focusing on the chemical basis of dietary selection while investigating the nutritional ecology of animals helps understand their feeding biology. It is also important to consider food abundance/biomass while studying the mechanism of animal food selection. We studied leaf selection in two Bornean folivorous primates in relation to plant chemistry and abundance: proboscis monkeys inhabiting a secondary riverine forest and red leaf monkeys inhabiting a primary forest. Both species tended to prefer leaves containing higher protein levels, although more abundant plant species were chosen within the preferred species, probably to maximise energy gain per unit time. However, the two species showed clear differences in their detailed feeding strategy. Red leaf monkeys strictly chose to consume young leaves to adapt to the poor nutritional environment of the primary forest, whereas proboscis monkeys were not highly selective because of the better quality of its common food in the riverine forest.

Regurgitation and remastication in the foregut-fermenting proboscis monkey (Nasalis larvatus)

Although foregut fermentation is often equated with rumination in the literature, functional ruminants (ruminants, camelids) differ fundamentally from non-ruminant foregut fermenters (e.g. macropods, hippos, peccaries). They combine foregut fermentation with a sorting mechanism that allows them to remasticate large particles and clear their foregut quickly of digested particles; thus, they do not only achieve high degrees of particle size reduction but also comparatively high food intakes. Regurgitation and remastication of stomach contents have been described sporadically in several non-ruminant, non-primate herbivores. However, this so-called ‘merycism’ apparently does not occur as consistently as in ruminants. Here, to our knowledge we report, for the first time, regurgitation and remastication in 23 free-ranging individuals of a primate species, the foregut-fermenting proboscis monkey (Nasalis larvatus). In one male that was observed continuously during 169 days, the behaviour was observed on 11 different days occurring mostly in the morning, and was associated with significantly higher proportions of daily feeding time than on days when it was not observed. This observation is consistent with the concept that intensified mastication allows higher food intake without compromising digestive efficiency, and represents an expansion of the known physiological primate repertoire that converges with a strategy usually associated with ruminants only.

A Bayesian analysis of the temporal change of local density of proboscis monkeys: Implications for environmental effects on a multilevel society

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.

Excretion patterns of solute and different-sized particle passage markers in foregut-fermenting proboscis monkey (Nasalis larvatus) do not indicate an adaptation for rumination.

Behavioral observations and small fecal particles compared to other primates indicate that free-ranging proboscis monkeys (Nasalis larvatus) have a strategy of facultative merycism(rumination). In functional ruminants (ruminant and camelids), rumination is facilitated by a particle sorting mechanism in the forestomach that selectively retains larger particles and subjects them to repeated mastication. Using a set of a solute and three particle markers of different sizes (b2, 5 and 8mm),we displayed digesta passage kinetics and measured mean retention times (MRTs) in four captive proboscis monkeys (6–18 kg) and compared the marker excretion patterns to those in domestic cattle. In addition, we evaluated various methods of calculating and displaying passage characteristics. The mean ± SD dry matter intake was 98 ± 22 g kg−0.75 d−1, 68 ± 7% of which was browse. Accounting for sampling intervals in MRT calculation yielded results that were not affected by the sampling frequency. Displaying marker excretion patterns using fecal marker concentrations (rather than amounts) facilitated comparisons with reactor theory outputs and indicated that both proboscis and cattle digestive tracts represent a series of very few tank reactors. However, the separation of the solute and particle marker and the different-sized particle markers, evident in cattle, did not occur in proboscis monkeys, in which all markers moved together, at MRTs of approximately 40 h. The results indicate that the digestive physiology of proboscis monkeys does not show typical characteristics of ruminants, which may explain why merycism is only a facultative strategy in this species.

A short note on seed dispersal by colobines: the case of the proboscis monkey

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.

Species Richness and Distribution of Primates in Disturbed and Converted Forest Landscapes in Northern Borneo

Knowledge of fundamental aspects of ecology such as species richness and distribution, and the factors affecting them, is increasingly used to identify priority areas for conservation and to effectively manage threatened species. We investigated the species richness and distribution pattern of nonhuman primate communities inhabiting 10 sampling sites in four different habitat classes corresponding to increasing habitat disturbance level, that is, old growth forest, twice logged forest, repeatedly logged forest, and oil palm plantation, in and around Kalabakan Forest Reserve, in central Sabah, Malaysian Borneo. By using direct and indirect survey methods, we confirmed the existence of 9 out of the total 10 primate species, found in Sabah, within the surveyed areas. Based on the monthly number of primate species detected, our results indicated a general trend of decreasing primate species richness with increasing habitat disturbance level. However, the response within the disturbed forest sites showed some variations with some sites in repeatedly logged forest displaying comparable primate species number to that of the undisturbed forest sites. We also found that within the forest habitats, tree density is a good predictor of the richness of the primate community with a positive effect. Hence, tree density may be a key indicator for evaluating primate communities in forest habitats. Overall, the results of our study suggest that although not equivalent to areas of undisturbed forest, degraded forests—including those that have been repeatedly logged—are still valuable for primate conservation. In contrast, oil palm plantations have mainly negative effects on the primate community.

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.