Social organization and ecology of proboscis monkeys (Nasalis larvatus) in mixed coastal forest in Sarawak

Data are presented from a 16-month study of proboscis monkeys in an area of mixed coastal forest in Sarawak. The population density, social organization, and feeding and ranging behavior are described in detail. Results are compared with those from other primates in an attempt to understand why females of certain species (including proboscis monkeys) transfer between social groups. The scarcity of available food and reasons for the limited habitat preferences of proboscis monkeys are also discussed.     

The mating system of the Sichuan snub‐nosed monkey (Rhinopithecus roxellana)

This article reports the first genetic study of the mating system of the Sichuan snub‐nosed monkey (Rhinopithecus roxellana), an endemic and endangered species in China. The investigation was carried out in a population (WRT) in the Qinling Mountains using data from both field observation and paternity analysis through microsatellite DNA profiling. During a mating season, a male on an average copulated with 5.7 females. Approximately 18% of the females were observed to copulate with more than one male over the study period. The majority of copulations (94.5%) were initiated by females. Twenty‐eight of 430 observed matings were extra‐unit copulations. Eight polymorphic microsatellite loci were used for paternity analysis. The number of alleles at each locus ranged from 3 to 7 (mean=4.3). Observed heterozygosity ranged between 0.32 and 0.79. None of the loci showed significant deviation from Hardy–Weinberg equilibrium. Results from paternity exclusion showed that 12 of 21 (57.1%) immature individuals were sired by extra‐unit males. Although the basic social unit of snub‐nosed monkeys is consistent with a polygynous mating system, both field observation and genetic data suggests that their mating system is polygamous. Infanticide and inbreeding avoidance are the most likely explanations for the promiscuity of female snub‐nosed monkeys. Am. J. Primatol. 72:25–32, 2010. © 2009 Wiley‐Liss, Inc.     

Comparison of diets fed to southeast Asian colobines in North American and European zoos,with emphasis on temperate browse composition

In May and June 1994 a survey of diets fed to captive southeast Asian colobines in European (n = 12) and North American (n = 9) zoos was conducted. Most diets were very complex, comprising an average of 25 ingredients; 149 different foods were listed in responses. Comparison of diets fed showed that European zoos feed a greater variety of fruits and vegetables, and fewer browse plants, than North American zoos. No standardized diet recommendations, based on ingredient or nutrient composition, are currently available for colobines in captivity. Foods eaten by these primates in nature appear to contain higher amounts of fiber and lower protein and soluble carbohydrates than current zoo diets. Temperate browse plants (n = 11 spp.; leaves plus twigs) sampled in New York in summer and autumn contained higher fiber and lower protein levels than diets fed in this survey, and may approximate the nutrient content of food items selected by free-ranging colobines. Fast-growing roses grown in greenhouses, fed primarily in Europe, contained substantially less fiber and higher protein concentrations than other browses offered, and may not be an appropriate substitute for native foods. © 1996 Wiley-Liss, Inc.     

Birth spacing in langur monkeys (Presbytis entellus)

This paper presents 10 years of reproductive data on birth interval length and 5 years of data on reproductive behavior postpartum from a captive colony of gray langur monkeys (Presbytis entellus)housed in Berkeley, California. Birth intervals of females following different pregnancy and nursing schedules are compared. Females whose infants survive to the age of 9 months have a median birth interval of 15.4 months. The experimental separation of mothers from infants for a period of 2 weeks, 6 to 9 months postpartum, had no significant effect on the median birth interval length. Females experiencing a pregnancy failure or the loss of a neonate had median birth intervals of 9.6 and 10.7 months, respectively. These intervals were significantly shorter than the birth intervals of females whose infants survived to 9 months, showing that the presence of a nursing infant delays the female’s time to next conception by approximately 5 to 6 months. Females experienced a median of three estrous periods (two estrous cycles) before conceiving postpartum, regardless of pregnancy outcome or length of infant survival, and females rarely conceived during their first estrous period postpartum. Weaning did not occur until after the mother’s next conception. These data indicate that, in populations of langurs characterized by average birth intervals of 15 to 16 months, the loss of an infant after the age of 5 to 6 months will not accelerate a female’s ability to conceive or shorten the birth interval length. The available data on birth spacing from populations of free-ranging langurs are reviewed. It could not be demonstrated that non-Himalayan populations are characterized by birth intervals which are as long as 20 to 24 months. Rather, it is suggested that female langurs inhabiting seasonally arid sites, such as Jodhpur, Abu, and Dharwar, may be capable of producing infants on the average of every 15 to 16 months. Flexibility in the timing of births and the lack of well-defined birth seasons at these sites may be explained by this species’ dietary and digestive adaptations. Additionally, data on birth spacing and the age of missing infants from the above field sites, where it has been suggested that infanticide following changes in male leadership occurs habitually, do not lend support to the sexual selection hypothesis of infanticide as proposed by S. Hrdy (1974, 1977).     

Dietary Profile of <Emphasis Type="Italic">Rhinopithecus bieti</Emphasis> and Its Socioecological Implications

To enhance our understanding of dietary adaptations and socioecological correlates in colobines, we conducted a 20-mo study of a wild group of Rhinopithecus bieti (Yunnan snub-nosed monkeys) in the montane Samage Forest. This forest supports a patchwork of evergreen broadleaved, evergreen coniferous, and mixed deciduous broadleaved/coniferous forest assemblages with a total of 80 tree species in 23 families. The most common plant families by basal area are the predominantly evergreen Pinaceae and Fagaceae, comprising 69% of the total tree biomass. Previous work has shown that lichens formed a consistent component in the monkeys’ diet year-round (67%), seasonally complemented with fruits and young leaves. Our study showed that although the majority of the diet was provided by 6 plant genera (Acanthopanax, Sorbus, Acer, Fargesia, Pterocarya, and Cornus), the monkeys fed on 94 plant species and on 150 specific food items. The subjects expressed high selectivity for uncommon angiosperm tree species. The average number of plant species used per month was 16. Dietary diversity varied seasonally, being lowest during the winter and rising dramatically in the spring. The monkeys consumed bamboo shoots in the summer and bamboo leaves throughout the year. The monkeys also foraged on terrestrial herbs and mushrooms, dug up tubers, and consumed the flesh of a mammal (flying squirrel). We also provide a preliminary evaluation of feeding competition in Rhinopithecus bieti and find that the high selectivity for uncommon seasonal plant food items distributed in clumped patches might create the potential for food competition. The finding is corroborated by observations that the subjects occasionally depleted leafy food patches and stayed at a greater distance from neighboring conspecifics while feeding than while resting. Key findings of this work are that Yunnan snub-nosed monkeys have a much more species-rich plant diet than was previously believed and are probably subject to moderate feeding competition.     

Parallel functional changes in the digestive RNases of ruminants and colobines by divergent amino acid substitutions

A morphological or physiological trait may appear multiple times in evolution. At the molecular level, similar protein functions may emerge independently in different lineages. Whether these parallel functional changes are due to parallel amino acid substitutions has been a subject of debate. Here, I address this question using digestive ribonucleases (RNases) of two groups of foregut-fermenting mammals: ruminant artiodactyls and colobine monkeys. The RNase1 gene was duplicated twice in ancestral ruminants at least 40 MYA, and it was also duplicated in the douc langur, an Asian colobine, approximately 4 MYA. After duplication, similar functional changes occurred in the ruminant and monkey enzymes. Interestingly, five amino acid substitutions in ruminant RNases that are known to affect its catalytic activity against double-stranded (ds) RNA did not occur in the monkey enzyme. Rather, a similar functional change in the monkey was caused by a different set of nine substitutions. Site-directed mutagenesis was used to make three of the five ruminant-specific substitutions in the monkey enzyme. Functional assays of these mutants showed that one of the three substitutions has a similar effect in monkeys, the second has a stronger effect, and the third has an opposite effect. These results suggest that (1) an evolutionary problem can have multiple solutions, (2) the same amino acid substitution may have opposite functional effects in homologous proteins, (3) the stochastic processes of mutation and drift play an important role even at functionally important sites, and (4) protein sequences may diverge even when their functions converge.     

A comparison of the floristics and leaf chemistry of the tree flora in two Malaysian rain forests and the influence of leaf chemistry on populations of colobine monkeys in the Old World

A comparative floristic survey of lowland tropical rain forest at Kuala Lompat, Krau Game Reserve, West Malaysia and at Sepilok Virgin Jungle Reserve, Sabah, East Malaysia, revealed significant differences in the composition of canopy species, notably in the relative paucity of Dipterocarpaceae and abundance of Leguminosae at Kuala Lompat. A further comparison with data from other sites in Malesia indicated that Kuala Lompat was rather atypical, representing an extreme example of the relatively legume rich and dipterocarp poor forests of West Malaysia. Conversely, the predominance of dipterocarps and lack of legumes at Sepilok was similar to other sites in Borneo. Young and mature leaves were collected from a representative sample of the canopy flora of the two study sites; the levels of nitrogen, fibre, total phenolics and condensed tannins, and degree of digestibility by cellulase and pepsin, were measured. Levels of fibre, nitrogen and phenolics differed significantly between the two floras; foliage from Kuala Lompat being, on the whole, richer in nitrogen but lower in phenolics and fibre. As a consequence of the lower levels of fibre, and less certainly of phenolics, the Kuala Lompat foliage was comparatively more digestible. Possible reasons for the differences in foliar biochemistry between the two sites are discussed. Differences in rainfall and in soil quality are regarded as potential evolutionary causes. A further comparison of the chemical profiles with data for other forests in India and Africa indicate that Sepilok is a site in which trees invest heavily in quantitative defences such as fibre and phenolics whereas trees at Kuala Lompat place a lower emphasis on the production of these. Finally, attention is drawn to the use of foliar chemical profiles in predicting the carrying capacity for colobine monkeys at each of the five Old World forests where data are available. It was found that the ratio of nitrogen to fibre correlated well with the biomass of colobines at the five sites.     

Tree leaf chemical characters: selective pressures by folivorous primates and invertebrates

Plants have evolved a variety of chemical means to deter herbivory. Several studies have documented that secondary compounds are strong deterrents to certain herbivores, while others have demonstrated that some herbivores ingest large quantities of these compounds without exhibiting deleterious effects. This inconsistent response suggests that plants have evolved compounds to deter specific herbivores. Based on a study in Kibale National Park, Uganda, we explored how two major groups of herbivores, invertebrates and colobus monkeys, respond to chemical characteristics of leaves: protein, attractive from a nutritional perspective, and alkaloids, saponins and cyanogenic glycosides, which are all plant defences, detering herbivory. The intensity that colobus monkeys fed on leaves of different tree species was determined by observations (1300 h), and invertebrate herbivory was indexed by collecting leaves from 20 species and digitizing tracings to quantifying invertebrate damage. Invertebrate damage to leaves varied among species (1.5–22.5%), but showed no relationship with saponin or protein content, or the presence or absence of alkaloids. Colobine foraging effort did not relate to the saponin and protein of leaf species, nor to the presence or absence of alkaloids. Prunus africana, the only species to test positive for cyanogenic glycosides, was fed on by colobus monkeys for 8.1% of their foraging time, but, as it occurred at low densities, it was the most preferred species. These results can be interpreted in different ways. First, it is possible that inactive compounds are retained because they increase the probability of producing new active compounds. Secondly, the indices used to evaluate compound effects may be inappropriate. For example, monkeys may only be able to tolerate a toxin to a specific threshold in a single feeding session, but our index of foraging effort was averaged over the year. Thirdly, it may be that these compounds play an active role with organisms not considered (e.g. prevent fungal attack). Finally, these compounds may serve some unknown function and selection may operate for that purpose.     

Postconflict Behavior of Spectacled Leaf Monkeys (Trachypithecus obscurus). I. Reconciliation

Studies of postconflict behavior have focused on Old World primates, particularly on members of the cercopithecines and chimpanzees. We present data on patterns of reconciliation in two captive groups of spectacled leaf monkeys, members of the Colobinae. Reconciliation occurred at a high rate relative to that in other primate species and within the first minute following a conflict. Friendly postconflict contact was usually initiated by aggressors in one group, and by recipients in the other. But, there was no difference in postconflict initiative to contact in comparison with MCs. These two groups showed behavioral specificity in the context of postconflict reunions. Ventroventral embracing was a common, explicit (de Waal, 1993) form of reconciliation. The intensity of aggression and situations in which the victim responded aggressively had no effect on the likelihood of reconciliation occurring. The postconflict behavior of both groups lends further support to the relationship-quality hypothesis (Aureli et al., 1989). Kinship and rank distance and had no effect on reconciliation, though affiliation levels correlated positively with the tendency to reconcile. These results indicate that spectacled langurs are among the more tolerant of the species studied so far.