The key distinction between these two approaches was that the food class analyses included changes in food availability over time, whereas the selectivity analyses did not; selectivity analyses included only measures of the commonness of stems. Despite the notable differences in dietary richness, both primates exhibited similar responses to variation in fruit availability. When fruit availability decreased, gibbons and leaf monkeys incorporated more leaves and figs into their diets, and when fruit availability increased they consumed more fruit and seeds. Below we briefly consider strengths and limitations of our methods, discuss how our results relate to what has been found for other populations of the same species in different habitats, and note how the results of our study fit more broadly in the context of other comparative studies of primate feeding ecology. Finally, we draw distinctions between selectivity analyses that are static and dynamic dietary composition analyses that incorporate temporal fluctuations in food availability. Using figs as an example, we discuss how a food source can paradoxically be identified as both a preferred and a fallback food, planting blueberries in pots and highlight the importance of taking variation in food availability into account when characterizing primate diets.We acknowledge that our sample sizes for feeding data are smaller than for most studies of primate feeding ecology, even those that are conducted over much shorter periods than ours.
Our sampling methods were a deliberate choice to ensure statistical independence, avoid pseudoreplication, and sample the population. Primate feeding data are typically collected during extended follows of focal animals and many feeding observations are recorded from the same group, often the same individual, on a single day. In addition, one or a small number of groups are typically sampled. These typical methods present challenges for appropriate statistical analysis, interpretation, and extrapolation beyond the sampled groups. Our methods place a primacy on ensuring statistical independence of feeding observations and avoiding biases associated with sampling few groups or habitat types. We note that while our sample sizes are small, they are unbiased, so the effects of small sample size are primarily on the width of confidence intervals and not the mean model results or general trends that we detected. While we consider our data to be an accurate representation of the feeding behavior of the populations of the two species we studied, certain limitations warrant consideration. For example, most of our feeding observations were made before noon, and there is evidence that some primate species alter their food intake over the course of the day. Spider monkeys in Santa Rosa National Park, Costa Rica, eat more fruit in the mornings, and more leaves during midday and in the evening.
Both siamangs and lar gibbons in Peninsular Malaysia show a similar pattern where they consume more leaves later in the day. If gibbons and leaf monkeys exhibit similar diurnal variation at our site, then our over-sampling of the morning would have biased our results. Sex and age can also have important influences on primate dietary composition. For example, in mountain gorillas , females and growing juveniles eat more food, and consume more protein per kilogram of body mass, than males. Significant differences in dietary composition between age and sex classes have also been described for sifakas , green monkeys , and snub-nosed monkeys . We collected feeding observations from the first individual detected along the transect line or a randomly selected focal animal, regardless of age or sex class, so there are no inherent biases in our methods towards certain types of individuals. Nevertheless, it is possible that certain age or sex classes are more easily detected along transects and would therefore be oversampled in the data. We have not detected significant differences in feeding observations from transects and randomly-selected focal follows , but note that our small sample sizes mean that our power to reject the null model of no difference is limited.We showed that gibbon and leaf monkey dietary overlap was asymmetrical and varied depending on the plant part consumed. Our results suggest that these primates are potentially important, albeit asymmetrical, food competitors, which is consistent with previous studies. For example, dietary overlap for leaves and seeds was high from the gibbons’ perspective but low from the leaf monkeys’ perspective.
This pattern was reversed for the dietary overlap for fruit, with leaf monkeys having a slightly higher measure of dietary overlap with gibbons than vice versa. Overall dietary overlap was higher from the gibbons’ perspective than from the leaf monkeys’ because leaf monkeys consumed a more diverse diet than gibbons did. Our dietary overlap analyses did not account for variation in resource availability or differences in habitat types due to limitations in sample size, but both these factors could potentially influence dietary overlap measures. For example, in three sympatric primate species in Santa Rosa National Park, Costa Rica, there was substantial variation in monthly dietary overlap measures. The authors propose that the high dietary flexibility of these primate species, along with variation in dietary overlap, means that feeding competition may only be an intermittent selective force, occurring on a supra-annual basis. Data from our site demonstrate that the different forest types support different densities of gibbons and leaf monkeys, and that degree of resource overlap between gibbons and other vertebrate frugivores varies substantially between peat swamps and other forest types. Importantly, our results of dietary overlap were consistent with results from other aspects of this study, showing that for the frugivorous portion of the diet, gibbons and leaf monkeys have similar measures of dietary overlap and dietary richness, but differences in dietary overlap and richness occur in the leaf and seed portion of the diet. Behavioral mechanisms, such as the incorporation of a broad range of foods in the diet, may allow folivorous primates such as leaf monkeys to reduce the amount of toxins consumed . By incorporating more varied food sources into their diets than gibbons, leaf monkeys at our site may mitigate the potential buildup of specific toxins from seeds and leaves, leading to greater diversity in the non-frugivorous portion of their diets. Fruits are easy to process and digest while leaves often contain antifeedants and other compounds that can be toxic to primates in large amounts. Unripe fruits are heavily chemically defended, possessing relatively high levels of anti-feedants and seeds also contain secondary compounds, such as strychnine and alkaloids, that can be toxic in large quantities. Our results are consistent with a recent study investigating dietary flexibility oftwo lemur genera, the omnivorous Eulemur, with the more folivorous Propithecus, raspberries in pots where anatomical adaptations to digest fiber allowed for increased dietary breadth in Propithecus .The results of the selectivity analyses provide further evidence that gibbons have a narrower diet than leaf monkeys, at least in the masting forests of CPRS. In line with our predictions, leaf monkeys preferred more genera and avoided fewer genera than gibbons. Both gibbons and leaf monkeys selected figs more than predicted based on their availability, when temporal variation was not considered. Interestingly, gibbons and leaf monkeys both avoided four of the same genera: Baccaurea, Calophyllum, Gironniera and Gymnacranthera.
These genera exhibit relatively low synchrony similar to figs, meaning that they are consistently available in the environment. For gibbons, the most important predictors of resource use are overall abundance of the genus, as well as the consistency of fruit availability. Although these four genera were relatively abundant, and consistently available, gibbons and leaf monkeys both avoided them, most likely because they are of low quality for primates . It is important to note that use or importance of a food item in a primate diet is different than preference, and genera that are classified as avoided may still constitute a substantial portion of the primate’s diet. This is because very common items may be consumed fairly often , but eaten much less often than would be predicted based on their availability . Despite methodological differences, both Marshall et al. and our selectivity analyses returned qualitatively similar results for gibbons. For example, both studies ranked the liana Artabotrys as being the most highly selected genus for gibbons. Artabotrys exhibits low synchrony, so it is consistently available. The high selectivity score for Artabotrys in both our study and previous studies indicates that gibbons are consuming this genus more than predicted based on availability, which is probably because it produces relatively high quality, sugar-rich fruits that are easy to process, as well as the fact that it is often available during periods of otherwise low food availability. Our selectivity results are also similar to those of gibbon hybrids in the Barito Ulu research area, Central Kalimantan, Indonesia.Both gibbons and leaf monkeys experienced dramatic fluctuations in resource availability during the study period. Fruit availability varied by more than an order of magnitude among months, from less than 1% of stems to over 15% of stems bearing fruit—to place these numbers in context, note that majority of trees that we have monitored in our plots never fruited in a seven-year period that included two mast fruiting events. Extreme fluctuations in fruit availability, which are unpredictable from the primate’s perspective, are important forces shaping primate behavior, ecology and morphology. It is therefore crucial to capture the full range of variation in fruit availability when studying primate diets. Our study encompassed at least one masting event- two for leaf monkeys due to random variation in sampling of the different primate species- which allowed us to compare the primate diets over the full range of resource availability they are likely to experience. Despite the fact that gibbons and leaf monkeys have distinctly different diets, their dietary response to decreased fruit availability was qualitatively similar. Both primates showed increased consumption of leaves when fruit was less abundant. A similar pattern was seen forfigs, with both primates increasing their fig consumption when fruit was less abundant, and eating very few figs during periods of high fruit availability. The patterns of leaf and fig consumption exhibited by gibbon and leaf monkeys indicate that they utilized these foods as fallback foods, as reported in analyses of earlier data sets at CPRS. We discuss how figs can be paradoxically identified as preferred and as fallback foods below. Our results are consistent with past studies conducted on leaf monkeys in masting forests on Borneo. In areas where resource availability is highly variable, leaf monkeys eat more leaves during periods of low fruit availability, but incorporate fruit into the diet when it is available. This dietary switching has not been shown to occur in non-masting forests. For example, leaf monkeys were shown to have a higher degree of frugivory in non-masting peat swamp forests of Sabangau, Central Kalimantan, Indonesia than those reported by other researchers in masting dipterocarp forests of Gunung Palung, Sepilok, Tanjung Puting and Danum Valley, and the amount of fruit included in the diet was not influenced by changes in overall fruit availability. Leaf monkeys did not incorporate low quality foods into their diets in the non-masting peat forests, as fruit was consistently available year-round. Although peat swamp forests are present at our study site, we excluded peat swamp forest from our investigation of the influence of fruit availability on dietary composition because combining feeding observations from masting and non-masting forests that were phenologically unsynchronized would have confounded the analysis. Our results supporting the occurrence of dietary shifts in response to food availability suggest that differences in dietary strategies used in peat swamp forests versus dipterocarp forests may be substantial. Both primate species in our study showed a marked increase in fruit consumption when fruit availability increased, and even during periods of fruit scarcity, fruit comprised at least 50% of gibbon diets, which is consistent with studies at other sites and previous studies at CPRS. The same pattern was seen with seed consumption, and this is most likely because seed and fruit availability are intrinsically linked. This may be because gibbons do not consume many leaves, regardless of fruit availability, as leaves rarely comprised more than 25% of their feeding observations. It is also possible that with more sampling, a stronger relationship between fruit availability and leaves would emerge. Our results are consistent with other comparative primate studies. For example, three sympatric new world primates showed high degree of dietary overlap during periods of high fruit availability when a few abundant fruit species dominated their diets, but during periods of low fruit availability their diets diverged, and they incorporated more fungus , nectar or arthropods into their diets.