Use of SSR fragment length homozygotes for orangutan systematics

The use of simple sequence repeat (SSR) loci lacking length polymorphisms among their alleles (defined here as homozygotes) in systemtic studies has thus far been largely ignored due to their apparent lack of genetic heterogeneity. However, in this paper we show that point mutations, insertions, and deletions within SSR loci of identical size can be highly informative for population genetic and evolutionary studies. Our preliminary study of the von Willebrand factor (vWF) locus shows that there is a significant level of divergence among the Bornean Orangutans which implies that present orangutan subbopulations in Borneo are genetically isolated from each other. However, our findings do not confirm that the Bornean and Sumatran Orangutans form two separate clades.     

Limits to food intake and fiber utilization in the prairie vole,Microtus ochrogaster: effects of food quality and energy need

We fed prairie voles (Microtus ochrogaster) rat chow diluted with variable amounts of -cellulose to determine 1) how much fiber the voles could tolerate in their diet; 2) changes in food intake and digestibility of dry matter and of fiber; 3) the extent to which voles utilized fiber as an energy source; and 4) whether any of these variables differed between groups of animals maintained at 5 or 22°C. Fiber content of the diets ranged from 20 to 84%. Animals held at 5°C maintained body mass through a diet containing 69% fiber, while animals held at 22°C maintained body mass through the 84% fiber diet. Dry matter intake increased with fiber level from 9.3 to 15.0 g·day^-1 for animals at 5°C and from 5.6 to 14.0 g·day^-1 for animals at 22°C; intake on the highest fiber diet eaten by either group was not different. Dry matter digestibility decreased significantly as the fiber in the diets increased, but was not affected by temperature treatments. Digestible dry matter intake for each group remained constant regardless of diet quality, but on each diet digestible dry matter intake for animals at 5°C was significantly higher than that of the animals held at 22°C. Digestibility of the fiber portion of the experimental diets remained constant as food quality decreased, so the percent of daily energy need met by fiber utilization increased with higher food intake. On the lowest quality diet each group tolerated, fiber digestion provided approximately 42 and 68% of the energy needs of voles at 5 and 22°C, respectively.Abbreviations BM body mass - BMR basal metabolic rate - DE digestible energy - DM dry matter - DMD dry matter digestibility - DDMI digestible dry matter intake - MR metabolic rate - NDF neutral detergent fiber (=cell walls) - NDS neutral detergent solubles (=cell solubles) - SEM standard error of mean - T _a ambient temperature     

Fragility of Traditions: The Disturbance Hypothesis for the Loss of Local Traditions in Orangutans

Chimpanzees and orangutans have increasingly well documented local traditions involving learned skillful behaviors, often involving tools, which vary from place to place and are maintained by social transmission. These local traditions are most likely the antecedents of human culture. The complexity of local traditions is thought largely to be a function of the cumulative frequency of opportunities for social learning, and hence of the extent of tolerant gregarious foraging. Data on orangutans and chimpanzees are consistent with this hypothesis. This reliance on continued social transmission makes local traditions vulnerable to interruptions of transmission. I examine the disturbance hypothesis, which suggests that local extinction, hunting pressure, selective logging, and habitat loss in general affect the key parameters of the transmission process—innovation, diffusion, horizontal transmission—and hence will significantly impoverish the repertoire of complex skills for subsistence. Given current trends in orangutan habitats, serious erosion of local traditions is taking place. I also speculate that disturbance in the past has led to a significant loss of orangutan traditions.     

The ontogeny of sexual dimorphism in the cranium of Bornean orang-utans (Pongo pygmaeus pygmaeus) as detected by principal-components analysis

The ontogeny of cranial sexual dimorphism in the Bornean orang-utan (Pongo pygmaeus pygmaeus) is examined by means of principal-components analysis (PCA). Normalized first components are called allometry vectors or vectors of relative growth and show that sexual dimorphism is present at all stages of growth. Two patterns of sexual dimorphism are present: (1) sexual differences at age groups 2 and 3 are the result primarily of differences in principal component II scores, reflecting mainly shape-related differences, and (2) age groups 5, 6, and 7 show a trend of stronger size-related shape differences with increasing age in the allometry vector along with decreasing differences in principal component II scores, reflecting an increase in size-related shape differences between the sexes. Age group 4 shows a combination of both patterns. Our results support Shea's hypothesis (1985a) that when using multigroup PCAs in closely related taxa, the allometry vector will generally estimate the shape variation resulting from the extension of common growth allometry patterns (ontogenetic scaling). The second and subsequent components summarize shape variation from slope and intercept differences between the groups, provided that ontogenetic scaling is not solely responsible for all the shape differences present. Subanalyses of those dimensions previously found to show ontogenetic scaling and acceleration follow this pattern well. The total sample provides a pattern whereby ontogenetically scaled dimensions possess a stronger influence over accelerated dimensions but still generally follow Shea's hypothesis. Finally, variously derived coefficients provided several interesting findings: (1) strong evidence was found against multivariate isometry for both the pooled and the separate samples, (2) multivariate allometric coefficients for both sexes follow the general growth pattern of negative scaling in neurocranial dimensions and positive scaling in the viscerocranium, and (3) multivariate slopes have a very high correlation with bivariate slopes relative to the same independent X variable, thereby lending further support to Jolicoeur's (1963a, b) allometry generalization.     

Modeling dietary selectivity by Bornean orangutans: Evidence for integration of multiple criteria in fruit selection

Food patch visitation was compared to the availability of fruit patches of different species during 2 years in a Bornean lowland forest to examine orangutan (Pongo pygmaeus) diet selectivity. Feeding on both the pulp and the seeds of nonfig fruit varied directly with fruit patch availability, demonstrating preference for these foods over fig fruit or other plant parts (bark or leaves). Factors determining fruit selectivity rank were examined through multiple regression analysis. Modeling selectivity for 52 chemically unprotected primate-fruit pulp species revealed strong preferences for species of (i) large crop size (numbers of fruits ripening in an individual patch), (ii) high pulp weight/fruit, and (iii) high pulp mass per swallowed unit of pulp + seed, demonstrating orangutan sensitivity especially to patch size (g of pulp or total energy/patch) and perhaps to fruit handling time. Modeling selectivity for 18 fig species showed that 4 factors significantly influenced fig species rank: crop size, pulp weight/fruit, and 2 chemical variables, percentage digestible carbohydrate and percentage phenolic compounds in the fig fruit pulp. The selectivity rank based on the overall nutrient gain from feeding in the fruit patch (the product of the first 3 variables) is proportionally depressed by the percentage tannin content, demonstrating that orangutans integrate values for these variables in selecting fig patches. The conclusions from these results and from analysis of selectivity for seeds and for other fruit types are that orangutan foraging decisions are strongly influenced by the meal size expected from a feeding visit (i.e., by patch size), that tannins and other toxins deter feeding, and that the energy content, rather than the protein content, of foods is important in diet selection. The foraging strategy of orangutans is interpreted relative to these results and to Bornean fruiting phenology. By integrating spatial, morphometric, and chemical variables in analysis, this study is the first to demonstrate the application of foraging theory to separate out the key variables that determine diet selection in a primate. Multivariate analysis should routinely be applied to such data to distinguish among the many covarying attributes of food items and patches; inferences drawn in previous studies of primate diet selection, which ignore key spatial and morphological variables and rely on univariate correlations, are therefore suspect.     

Hand preferences in captive orangutans (Pongo pygmaeus)

The strength of the evidence for population-level handedness in the great apes is a topic of considerable debate, yet there have been few studies of handedness in orangutans. We conducted a study of manual lateralization in a captive group of eight orangutans (Pongo pygmaeus) ranking the degrees of manual preference according to a defined framework. We analyzed five behavioral patterns: eat (one- and two-handed), make/modify tool, oral tool-use, and manual tool-use. Although some individuals showed significant manual preferences for one or more tasks, at the group-level both one-handed and two-handed eating, oral tool-use, and make/modify tool were ranked at level 1 (unlateralized). Manual tool-use was ranked at level 2, with four subjects demonstrating significant hand preferences, but no group-level bias to the right or left. Four subjects also showed hand specialization to the right or left across several tasks. These results are consistent with most previous studies of manual preference in orangutans. The emergence of manual lateralization in orangutans may relate to more complex manipulative tasks. We hypothesize that more challenging manual tasks elicit stronger hand preferences.     

Paternity determination in captive lowland gorillas and orangutans and wild mountain gorillas by microsatellite analysis

Paternity exclusion studies provide useful information for testing certain theories of behavioral ecology and for the management and conservation of both wild and captive populations of endangered species. This study used eight human nuclear microsatellite loci, in the absence of species-specific PCR primers, to genetically identify the sires of 12 captive lowland gorillas (Gorilla gorilla gorilla) and 2 captive orangutans (Pongo pygmaeus pygmaeus andPongo p. abelii). Parentage assignments were confirmed by excluding all except a single potential sire for each offspring with the least two loci. Sire-offspring relationships were verified in 12 of the 14 cases, and reassigned in the case of two gorilla offspring. The orangutan paternity typing was supplemented by DNA fingerprinting. Additionally, five of the eight microsatellite loci, in conjunction with behavioral data, were used for a non-exhaustive set of paternity exclusions for five wild mountain gorillas (Gorilla g. beringei). The eight loci described in this study should be useful additions to the tools available for the study of genetics in the great apes.     

Food selection by the silver leaf monkey,Trachypithecus auratus sondaicus,in relation to plant chemistry

Summary Samples of leaves and fruits exploited as food items byTrachypithecus auratus sondaicus were analysed for nitrogen content, acid detergent fibre (ADF), pepsin cellulase digestibility (CDIG), condensed tannins (CT), total phenolics (TP) and protein precipitation capacity (PP) and compared with fruits and leaves not eaten. Differences in chemical measures for items eaten and not eaten were not statistically significant but trends indicate that leaves may have been selected for their lower fibre content and greater digestibility. Fruits eaten also had a higher mean level of CDIG and lower mean level of ADF than fruits not eaten but these measures are not considered to be of major importance in fruit selection as CDIG was lower and ADF higher in fruits eaten than in leaves eaten. Levels of CT, TP and PP capacity were higher in fruits eaten than in fruits not eaten but lower in leaves eaten than in leaves not eaten. The role of tannins and phenolics in food selection is discussed. Leaves (and fruits) were not strongly selected on the basis of protein content. Approximately half the dietary intake ofT. auratus sondaicus was leaves, a protein-rich food source. Possibly, protein levels in foliage at Pangandaran were sufficient that selection for this nutrient was not required. A nutrient other than protein (for example, soluble carbohydrates) may have been maximised through food selection. The protein/ADF ratio may provide an indicator of the acceptability of foliage in a habitat as potential food for a colobine. However, this ratio did not govern food selection byT. auratus sondaicus at Pangandaran.     

The role of taste in food selection by African apes: implications for niche separation and overlap in tropical forests

Ripe fruit eating shapes the behavior of most of the apes. Gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes) are very different sizes and, consequently, have been traditionally viewed as ecologically distinct, but few studies have explored the behavioral and physiological foundations of their diets. Debate continues on the extent that large-bodied gorillas may be less selective and more opportunistic fruit eaters than chimpanzees. Taste responses have been predicted to relate to body size and digestive strategies. This study employs laboratory research on taste perception and discrimination among captive zoo-housed chimpanzees and relates it to previous work on gorillas to better characterize diets and niche separation among these apes. During the captive trials, differences were recorded in consumption patterns of water and varying concentrations of dilute aqueous fructose (sweet) and tannic acid solutions (astringent), compounds commonly found in wild foods. The chimpanzees exhibited similar preference thresholds for fructose (50 mM) to other primates studied. They exhibited slightly lower inhibition thresholds for tannic acid solutions than gorillas, but higher than smaller primates studied to date. These preliminary findings suggest that tannin tolerance may well be mediated by body size, though possible species differences in salivary proteins or other sensory differences remain to be explored. This research furthers our efforts to understand the roles of body size and physiological adaptations in shaping diet and niche separation of chimpanzees and gorillas.     

Ecological constraints on the grouping of wild orang-utans (Pongo pygmaeus) in the Gunung Leuser National Park,Sumatra, Indonesia

The orang-utan (Pongo pygmaeus)is an interesting subject on which to base an evaluation of the costs and benefits of social life in apes, since grouping in this heavy, arboreal frugivore is facultative. In the Ketambe area of Sumatra, Indonesia, the food sources of wild orang-utans display a clear seasonality. The two main food types— figs and other, nonfig, fruits— fulfill different functions. The huge fig trees meet the high caloric requirements of the ape and are therefore visited regularly throughout the year. Nonfig fruits are an additional food source but become a really important alternative when figs are in short supply. Since fig trees are relatively rare, it is only in the nonfig fruiting season that food is relatively abundant. Two types of orang-utan groupings could be distinguished. During lean periods, groups formed in the few productive fig trees available can be explained as forced aggregations taking place in spite of centrifugal forces caused by competition. Only when a temporary surfeit of food slackens these centrifugal forces (i.e., during the fruit season) does the tendency to form spontaneous social groups (the second type of grouping) reveal itself. It is suggested that the development of social skills is an important aspect of grouping in adolescent orang-utans. For the adult male, safeguarding his reproductive success by protecting females against sexually aggressive subadult males is probably the only reason for being in groups.     

Digesta retention in the gastro-intestinal tract of the orang utan (Pongo pygmaeus)

The diet of the orang utanPongo pygmaeus consists of fruit, leaves, communal insects, and bark, and contains appreciable amounts of non-starch polysaccharides. These complex carbohydrates require microbial fermentation before they can be used as an energy source by the orang utans. The gastrointestinal tract ofP. pygmaeus consists of a simple or unipartite stomach, a relatively long small intestine, and a complex haustrated caecum and colon. This morphology suggests that the capacious proximal colon is the principal site of digesta retention and fermentation of non-starch polysaccharides. We measured several parameters of digesta retention by giving three captive adultP. pygmaeus a pulse dose of inert markers specific for the solute and particulate phases of the digesta and collected their faeces at regular intervals over 192–338 hours. Transit times (times of first appearance of the markers in the faeces) and mean retention times (MRT) were long, consistent with a large complex gastro-intestinal tract. MRTs for the particulate marker were longer (p=0.032) than for the solute marker, indicative of selective retention of large particulate digesta. These results are consistent with the patterns of marker excretion in other mammals that use the digestive strategy of colon fermentation.     

A report of behavioral lateralization in an infant orang-utan (Pongo pygmaeus)

The limb used to perform seven common activities was recorded during weekly observations of an infant orang-utan. For five of these behaviors, preferences were found that remained consistent in their direction, although there were week to week fluctuations in magnitude. Most notably, a right hand preference was found for nonfood reaching and a right hindlimb preference appeared for initiating locomotion. Although initially, food reaching was predominantly with the right hand, a shift toward preferential left hand use occurred during the final weeks of the study. Additionally, a left hand preference appeared when the infant touched either its body or head.     

Food plant selection by reindeer during winter in relation to plant quality

The relative palatabilities of nine plant taxa used as winter food by reindeer were estimated by presenting them in cafeteria and pairwise tests Feeding p reference indices were then related to the chemical composition of the plants High preference indices were obtained for the lichens Bryoria spp, Cladina arbuscula, C rangiferina and C stellaris, while low values were obtained for the moss Pleurozium schrebel and the dwarf shrubs Empetrum hermaphroditum and Vaccinium myrttllus The grass Deschampsia flexuosa and the lichen Stereocaulon paschale received intermediate scores Feeding preferences showed a strong negative correlation with acid detergent fiber (ADF)-values No statistically significant correlations were found between feeding preferences and contents of nitrogen, in vitro organic matter digestibility (IVOMD) or neutral detergent fiber (NDF)     

A simple, integrative assay to quantify nutritional quality of browses for herbivores

Many regard the concentrations of nitrogen (N), tannins and plant cell wall constituents (fibre) as key indicators of food quality and habitat suitability for browsing herbivores; yet there is no method for measuring their combined effects. We have developed a simple in vitro assay for measuring the effects of tannins and fibre on N availability in browse. We determined the effects of tannins by measuring the polyethylene glycol (PEG)-binding capacity (PEG-BC) of Eucalyptus leaf samples, followed by a two-stage in vitro digestion with pepsin and cellulase to determine the digestibility of dry matter and N. There was a significant relationship between concentrations of digestible N and the PEG-BC of the leaves. Furthermore, adding PEG significantly improved the digestibility of N. Our results concur with in vivo observations from several mammalian species. This suggests that our method is effective for measuring the nutritional quality of browse and the benefits of adding PEG, providing some index of the detrimental effects of tannins. We further simplified the assay by removing the PEG step, allowing us to quickly analyse samples in bulk. Nevertheless, this simplified method is still not practical for analysing the many samples necessary to compare the nutritional values of different tracts of forest. We used near-infrared reflectance spectroscopy to produce calibration equations and predicted total and digestible N in 322 trees at eleven sites. Both within and between sites, we found a wide variation in concentrations of digestible N but a much lower variation in total N, with either no relationship or poor relationships between the two measures. This confirms the variability in the nutritional quality of eucalypt forests, which may explain the distribution and abundance of mammalian herbivores. Thus, our assay provides a useful tool for understanding how food resources influence herbivore populations at different scales. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Orangutan Nesting Behavior in Disturbed Forest of Sabah,Malaysia: Implications for Nest Census

High concentrations of orangutans remain in the multiple-use forests of the Lower Kinabatangan, Sabah, Malaysia. Compared to primary forest, the habitat is highly fragmented, characterized by a low tree density (332 stems/ha), small tree size (83.6% of trees are <20 m high), low basal area (18 m²/ha), abundance of canopy gaps and high level of soil disturbance. The forest structure and composition influence orangutan nesting patterns, and thus directly influence the results of nest surveys used to determine orangutan population size. In logged forests, tall and large trees are the preferred nesting sites of orangutans. The scarcity of suitable nesting sites in the logged-over forests of Kinabatangan, could partly explain the lower daily rate of nest construction (r = 1.00) versus those of other orangutan populations. The nest decay rate t recorded at the study site (average ± SD = 202 ± 151 days) strongly depends on the species of tree in which a nest is built. Our results illustrate that the nest-related parameters used for orangutan censuses fluctuate among habitat types and emphasize the need to determine specific values of r for specific orangutan populations and of t for different tree species in order to achieve accurate analysis of census data.     

Aspects of dental development in the orangutan prior to eruption of the permanent dentition

In spite of a resurgence of interest in the interpretation of the sequences of dental development and eruption in various Plio-Pleistocene hominoids as being either “modern human” or “ape-like,” the body of comparative material on the extant hominoids remains deficient in critical areas. In concert with recent attempts to rectify this situation, we present the results of our studies on dental morphogenesis in the orangutan. We have focused on the growth and eruption of the deciduous dentition as well as early stages of permanent tooth formation and have found that 1) many permanent teeth develop earlier than was thought, 2) differences exist between development in the upper and in the lower jaw, and 3) states of tooth formation can vary significantly among individuals of similar chronological age or tooth eruption status.     

Patch selection by red deer in relation to energy and protein intake: a re-evaluation of Langvatn and Hanley's (1993) results

Langvatn and Hanley (1993) recently reported that patch use by red deer (Cervus elaphus) was more strongly correlated with short term rates of intake of digestible protein than dry matter. Such short term measures overlook effects of gut filling, which may constrain intake by ruminants over longer time scales (i.e., daily rates of gain). We reanalyzed Langvatn and Hanley's data using an energy intake model incorporating such a processing constraint, to determine whether their conclusions are robust. We found that the use of patches by red deer was just as strongly correlated with an estimate of the daily rate of intake of digestible energy as one of digestible protein during four out of seven trials, but slightly lower in three out of seven trials. In all cases, daily intake of digestible energy was a much better predictor of patch preference by red deer than was the intake of dry matter. Our reanalysis suggests that the daily intake of energy was highly correlated with that of protein in these trials, as may often be the case for herbivores feeding on graminoids. Hence the observed pattern of patch use by red deer could simultaneously enhance rates of both protein and energy intake.     

The chemical composition of pine foliage in relation to the population dynamics of the pine beauty moth,Panolis flammea,in Scotland

Summary This paper reports part of a study to determine why damaging outbreaks of the pine beauty moth, Panolis flammea (D & S) (Lepidoptera: Noctuidae), in Scotland are frequent on lodgepole pine but do not occur on Scots pine, and why outbreaks on lodgepole pine are mainly confined to trees growing in deep unflushed peat. The elongation of shoots and the growth of needles of Scots pine occurred later in the season than did those of lodgepole pine. The foliage of Scots pine generally had a higher level of nitrogen, and consistently had a higher level of phosporus, but had a consistently lower level of tannins than that of lodgepole pine during the period when the larvae were feeding each year. The nitrogen content of the foliage of lodgepole pine growing in an iron pan soil was generally higher than that of lodgepole pine growing in deep peat during the same period but there were no general differences in the phosphorus or tannin contents of lodgepole pine in the 2 soil types. These findings suggest that Scots pine is a more suitable host plant than lodgepole pine and that the foliage of lodgepole pine growing in deep peat is not more suitable than lodgepole pine growing in an iron pan soil. On the basis of the chemical analyses used in this study, it is concluded that the abundance of pine beauty moth in Scotland is not strongly influenced by the nutritional suitability of its host plants.     

Lifetable demography of four cladoceran species in relation to algal food (Chlorella vulgaris) density

Algal food density is known to influence life history variables of cladoceran species. It is not, however, well established whether both littoral and planktonic cladocerans show similar trends when exposed to increasing food concentrations. In the present work, we studied the life table demography of four cladoceran species (Ceriodaphnia cornuta, Moina macrocopa, Pleuroxus aduncus and Simocephalus vetulus) in relation to three algal food concentrations (low: 0.5 × 10⁶, medium: 1.5 × 10⁶ and high: 4.5 × 10⁶ cells ml^–1 of Chlorella vulgaris) (in terms of carbon content, these were equivalent to 0.15, 0.45 and 1.35 g ml^–1, respectively) at 25 °C. In general, for all the tested cladoceran species, values of average lifespan, gross reproductive rate, net reproductive rate, generation time and the rate of population growth were higher at lower food concentrations. Furthermore, high food concentration resulted in a negative population growth rate (mean ± standard error: –0.091 ± 0.026) for P. aduncus. The highest population growth rate (0.602 ± 0.014) was recorded for M. macrocopa at low food density. S. vetulus had the longest average lifespan (40 ± 1 d) while M. macrocopa had the lowest (5 ± 1 d). C. cornuta showed better performance at medium food concentration. We conclude that among the algal concentrations used here, 0.5 × 10⁶ – 1.5 × 10⁶ was beneficial not only to the planktonic species but also to the littoral P. aduncus and S. vetulus while 4.5 × 10⁶ cells ml^–1 was unsuitable for all the cladocerans tested.     

A comparative study of the food niches of lake-dwelling triclads and leeches

The food niches of four species of triclads and three species of non-parasitic leeches living in the littoral zone of British lakes of different trophic status were investigated, over one year, using a serological technique. Antisera against ten potential prey groups were employed. The basic data were adjusted to compensate for differences in predator size and seasonal changes in field temperatures. Data on two of the leech species have been presented elsewhere, but comparisons of the diet of all seven predator species are made in this paper. Much overlap in diet between the various predator species occurs, but, with one exception, each of the genera has a major food resource. The Polycelis spp. feed extensively on oligochaetes, Dugesia polychroa on molluscs, Dendrocoelum lacteum on Asellus, Erpobdella octoculata on chironomids and Glossiphonia complanata on molluscs. Helobdella stagnalis is a generalist feeder. Problems of coexistence of the leech species, and of the leech and triclad species are discussed.