Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Nutritional Differences between Two Orangutan Habitats: Implications for Population Density

  • Erin R. Vogel ,

    erin.vogel@rutgers.edu

    Affiliation: Department of Anthropology, Rutgers University, New Brunswick, New Jersey, United States of America

  • Mark E. Harrison,

    Affiliations: Department of Geography, University of Leicester, Leicester, United Kingdom, The Orangutan Tropical Peatland Project, Palangka Raya, Indonesia

  • Astri Zulfa,

    Affiliation: Fakultas Biologi, Universitas Nasional Jakarta, Jakarta, Indonesia

  • Timothy D. Bransford,

    Affiliation: Department of Anthropology, Rutgers University, New Brunswick, New Jersey, United States of America

  • Shauhin E. Alavi,

    Affiliation: Department of Anthropology, Rutgers University, New Brunswick, New Jersey, United States of America

  • Simon Husson,

    Affiliation: The Orangutan Tropical Peatland Project, Palangka Raya, Indonesia

  • Helen Morrogh-Bernard,

    Affiliation: The Orangutan Tropical Peatland Project, Palangka Raya, Indonesia

  • Santiano,

    Affiliations: The Orangutan Tropical Peatland Project, Palangka Raya, Indonesia, Centre for the International Cooperation in Sustainable Management of Tropical Peatlands, Palangka Raya, Indonesia

  • Twentinolosa Firtsman,

    Affiliations: The Orangutan Tropical Peatland Project, Palangka Raya, Indonesia, Centre for the International Cooperation in Sustainable Management of Tropical Peatlands, Palangka Raya, Indonesia

  • Sri Suci Utami-Atmoko,

    Affiliation: Fakultas Biologi, Universitas Nasional Jakarta, Jakarta, Indonesia

  • Maria A. van Noordwijk,

    Affiliation: Anthropological Institute and Museum, University of Zurich, Zurich, Switzerland

  • Wartika Rosa Farida

    Affiliation: Research Center for Biology, Indonesian Institute of Sciences (LIPI), Cibinong-Bogor, Indonesia

Nutritional Differences between Two Orangutan Habitats: Implications for Population Density

  • Erin R. Vogel, 
  • Mark E. Harrison, 
  • Astri Zulfa, 
  • Timothy D. Bransford, 
  • Shauhin E. Alavi, 
  • Simon Husson, 
  • Helen Morrogh-Bernard, 
  • Santiano, 
  • Twentinolosa Firtsman, 
  • Sri Suci Utami-Atmoko
PLOS
x

Abstract

Bottom-up regulatory factors have been proposed to exert a strong influence on mammalian population density. Studies relating habitat quality to population density have typically made comparisons among distant species or communities without considering variation in food quality among localities. We compared dietary nutritional quality of two Bornean orangutan populations with differing population densities in peatland habitats, Tuanan and Sabangau, separated by 63 km. We hypothesized that because Tuanan is alluvial, the plant species included in the orangutan diet would be of higher nutritional quality compared to Sabangau, resulting in higher daily caloric intake in Tuanan. We also predicted that forest productivity would be greater in Tuanan compared to Sabangau. In support of these hypotheses, the overall quality of the diet and the quality of matched dietary items were higher in Tuanan, resulting in higher daily caloric intake compared to Sabangau. These differences in dietary nutritional quality may provide insights into why orangutan population density is almost two times greater in Tuanan compared to Sabangau, in agreement with a potentially important influence of diet quality on primate population density.

Introduction

Bottom-up regulatory factors (e.g. nutrient availability, diet quality) are proposed to exert a strong influence on mammalian population density [17]. Studies relating habitat quality to primate population density have typically compared species or communities from distant sites [1,810], and the few studies that have quantified habitat quality at small spatial scales have examined food abundance without considering the energy available in food among the different populations [1116]. Recently, research on two different mountain gorilla populations found that differences in habitat-wide energy availability did not lead to difference in energy intake except during the high fruit period [17]. This is not surprising given that these two populations consume food items of similar nutritional content [18]. Those studies that have examined the relationship between the nutritional composition of diets and population density in primates have focused mostly on folivorous primates [9,1923], with very few studies focusing on frugivorous primates [24,25]. However, given that the majority of primate species are primarily frugivorous [26,27], fruit is typically much more energy rich than leaves [2830], and different levels of reliance on high quality fruits impacts primate densities [31], studies focusing on primates with more varied diets may provide greater insights into the influence of bottom-up factors on primate populations.

Elevated nutritional requirements associated with gestation and lactation are a major limiting factor to female reproductive success in mammals [3234]. Among primates, increased access to high quality food resources has been linked to reduced inter-birth intervals (IBI) in wild long-tailed macaques [35], baboons [36], langurs [37], and chimpanzees [3841]. Captive orangutans have been shown to have shorter IBIs relative to their wild counterparts, presumably due to consistently high nutritional intake [42]. In general, orangutans have extremely slow life histories, with the longest inter-birth intervals, lactation periods, and juvenile dependency of any non-human primate [4347]. Thus, all else being equal, variation in the nutritional quality of the diets of orangutan populations can result in increased reproductive success among females and ultimately impact population density [44,48].

The Bornean orangutan, Pongo pygmaeus wurmbii, provides an ideal species to study the relationships between dietary quality and population density. While primarily frugivorous, orangutans consume a variety of other plant items in their diets including insects, leaves, cambium, flowers, and other items [29,4951], which vary in nutritional composition and energetic returns [28,29,52]. Bornean orangutans show dramatic fluctuations in daily caloric intake in response to fruit availability, entering into negative energy balance states during low fruit periods [29,52,53]. Furthermore, Bornean orangutans are not subject to notable mortality risk from predators [54], other than humans [55], thus diminishing the effect of natural top-down predator regulation of population density. Orangutan population density has been shown to vary markedly across and within habitat types and, while fruit productivity is thought to influence density [56,57], the proximate factors underlying this variation have not been investigated.

The tropical peat-swamp forests of Central Kalimantan, Borneo hold the largest remaining populations of orangutans [5860], and show less pronounced fluctuations in fruit availability relative to dryland and riverine forests [3], as they do not experience the mast fruiting events that occur in more Dipterocarpaceae dominated dryland forests in the region [61]. The majority of peatlands in southern Borneo are ‘ombrogenous’, meaning that they acquire their nutrients almost exclusively through aerial precipitation and plant nutrient availability is low, as a product of this plus the typically flooded conditions [62,63]. In Sabangau, tree height, flora and fauna diversity, and orangutan density are known to vary in relation to peat depth and subsequent flooding regimes, which is thought to be linked to differences in peat nutrient availability [58,62,64]. However, there is great geographical variation in peatland ecology in Indonesia, with both peat depth [65] and the level of nutrient influx from river flooding varying substantially in the region [62].

Here, we compare the nutritional composition of plants consumed by two populations of wild orangutans in two distinct peatland habitats. The Sabangau Forest, including the research camp location, is a true ombrotrophic bog with limited nutrient input from aerial precipitation only. While the majority of the Mawas Conservation Area is similarly ombrotrophic, the Tuanan research station is located in a seasonally rheotrophic part of the area, with both shallower peat and a more alluvial flooding regime [66], and thus receives nutrients from seasonal river flooding, in addition to aerial precipitation [62,67]. In isolation, these differences would both be expected to result in higher forest fruit productivity in the Tuanan research area (cf. [62]). Because these two sites are also geographically close and climatically similar [68], any observed variation in fruit availability is likely due to differences in nutrient availability arising from these environmental differences. Finally, orangutan population density estimates between these two sites differ substantially, with Sabangau’s density estimated at 2.3 individuals/km2 [56] and Tuanan’s estimated at 4.3–4.5 individuals/km2 [56,69].

To explore if orangutan population density is related to variation in plant macronutrients and forest productivity, we systematically compared the nutritional composition of foods consumed by orangutans in these two Bornean peat-swamp forest sites. We predicted that (1) the nutritional composition of plant species in the site with shallower peat, a more alluvial flooding regime, and higher orangutan population density (Tuanan), would be of higher quality, resulting in (2) higher daily caloric intake in that site. In addition, we predicted that (3) forest productivity, measured in terms of the percentage of fruiting trees, would be greater in Tuanan.

Materials and Methods

Study Sites

Data were collected in the Sabangau (2° 19’ S and 113° 54’ E) and Tuanan (2°09’ S and 114°26’ E) research stations in Central Kalimantan, Indonesia, which are separated by 63 km and two major rivers (S1 Fig). The orangutan study grid in Sabangau has a peat depth of 1–4 m [62] and is located within the 500 km2 Natural Laboratory of Peat-swamp Forest (NLPSF), in the north-east of the 6,300 km2 Sabangau Forest. The Tuanan study area has a peat depth of 1–2 m in most parts, and overall ≤ 3.5 m [70], and is located in the 3,099 km2 Mawas Conservation Area, along the Kapuas Murung River. Both sites are recovering from selective commercial logging during the 1990s and subsequent illegal logging until the early 2000’s. Tree species composition in both sites is similar, although absolute and relative abundances of different species vary between the sites [71].

Orangutan Behavior

Data were collected on wild orangutans (Pongo pygmaeus wurmbii) at both sites from 2003–2010 following standardized orangutan protocols [72,73]. Although these populations are separated by two rivers and are genetically distinguishable subpopulations, they both belong to the Central Kalimantan population of Pongo pygmaeus wurmbii [74,75]. Focal-animal sampling was used and only data from all-day, nest-to-nest follows on independent, adult, habituated animals were included in the analyses (Sabangau n = 636 (6977 hrs.); Tuanan, n = 2233 (25,505 hrs.); see S1 Table). Feeding rates (number of items consumed /minute; area of cambium and phloem consumed/minute for bark) were collected from August 2005-June 2007 at Sabangau [52] and July 2005–2010 at Tuanan. Feeding rates did not differ between sexes in Sabangau [52] or Tuanan (Wilcoxon paired signed rank, S = -16.5, n = 33, p = 0.79; paired by plant species and food item) and thus average feeding rates obtained for other age-sex classes were used when computing energy intake if no data were available for a particular age-sex class (see below). From the standardized data, we calculated total minutes feeding on fruit and total follow length for each focal animal. Observational protocols were approved by IACUC committees of UC-Santa Cruz (protocol #20061056–122204) the George Washington University (protocol #A186), and Rutgers University (11–030).

Ecological Data Collection

Fruit availability.

Monthly phenology data collection at each site started in 2003 using near identical methods [71,73,76]. All trees with a diameter at breast height (DBH) of >10cm were monitored each month for the presence/abundance of fruit. An average of 1344 trees covering 2.4 ha in Sabangau and 1868 trees covering 2.3 ha in Tuanan were monitored. Tree species were identified by skilled local botanists and consistency of identifications across sites was checked by cross visits of researchers from both sites [71]. A fruit availability index (FAI) was calculated as the percentage of fruiting trees in the plots each month, and used as a proxy for forest productivity. To examine site differences in the availability of fruit and energy intake among the high and low fruit periods, monthly FAI scores were converted to z-scores and months with z < -1 were assigned into the low category, -1 ≤ z ≤1were assigned to the medium category, and z > 1were assigned to the high fruit category [following 3]. Stem density (number of stems per hectare) of matched species was also calculated from phenology plots at each site [71].

Plant sample collection, nutritional analyses and energy intake calculations.

Food samples were collected from July 2005-June 2007 in Sabangau and from June 2004-September 2010 in Tuanan by climbing trees and/or by collecting fresh fruit that had fallen from the tree. Wherever possible, samples were collected from trees in which orangutans had been observed feeding, were matched for the stage of ripeness that the orangutans consume, and were collected from multiple trees (2–10) to account for variation in nutrient content between trees of the same species [77]. Following previous terminology [52], we refer to a specific food species-part combination as a “food item”.

Samples were brought back to camp that day and processed [28,29,52]. We counted the number of pieces of each food item in the collected samples for each species (area for inner-bark), separated samples into parts ingested and discarded based on our observations of orangutan feeding at each site, and then dried the ingested parts of each sample at 30–50°C. Once dry, samples were weighed to obtain a field-dry weight. The field dry-weight per item was calculated then by dividing this value by the number of items in the original sample. Dried samples were stored with silica gel until they were shipped for nutritional analyses.

All nutritional analyses on plant foods from each site were conducted in the Laboratory of Nutrition Testing, Research Center for Biology, Indonesian Institute of Sciences (LIPI), Cibinong—Bogor, Indonesia following [52], unless noted below. Crude protein was determined using the Kjeldahl procedure for total nitrogen, which was then multiplied by 6.25 [78]. Crude lipid content was determined by the Soxtec method using Soxtex System HT2 as described in [79]. The detergent system of fiber analysis was used to quantify neutral-detergent fiber (NDF) [80,as modified by 81] and total non-structural carbohydrates (TNC) were calculated by difference [28]. We used published values for invertebrate (termite and ant) nutritional composition [82,83]. Dry matter (DM) and organic matter (OM) were calculated following [28]. All results are reported as the percentage of organic matter (OM).

Standard conversion factors were applied to the nutritional fractions to calculate metabolizable energy content per food item (ME kcal/100g OM = (4 x %TNC) + (4 x %CP) + (9 x %lipids) + (0.543 x %NDF), using the lower NDF digestion coefficient as recommended by [28]. Studies focusing on orangutan energetics have used different digestion coefficients for NDF [28,29,52]. In a digestion and passage experiment on chimpanzees, Milton and Demment [84] found that chimpanzees digested 54.3% of the NDF fed to them from biscuits containing 34% NDF, indicating a digestion coefficient of 0.543. This, value of 34% is the same as the average NDF reported for orangutan foods consumed in the wild [28]. Although we opted for use of the lower digestion coefficient in this study, it is important to note that analyses run with the higher digestion coefficient [cf. 52], did not alter the direction or significance of results (see S2 Table). Metabolizable energy per plant item was then calculated by multiplying the amount of energy per 100g OM by the dry weight of the item.

Energy intake per feeding bout was calculated following [52]. Feeding bouts were summed across the day to obtain total daily caloric intake (Kcal). If nutritional data and/or feeding rates were not available for a given plant species, we took either 1) data from a species of the same genus that was similar in fruit size/character, or where this was not available 2) the average value for a given item category (fruit, leaves, inner-bark, flowers, vegetation) and stage of maturity. This accounted for only 19.4% of the feeding bouts (3,542 out of 18,235) and 14.7% (100,842 out of 684,348) of feeding minutes for Tuanan and 29.6% (2,951 out of 9,885) feeding bouts and 19.1% (38,218 out of 199,675) of feeding minutes for Sabangau. Nutritional analyses were conducted on 221 species/parts from Tuanan and 183 from Sabangau [85].

Data analyses

To examine site differences in nutritional and energetic composition (ME) of all dietary items for which nutritional data were available set at each site, Wilcoxon Signed Rank Tests were used. The species included in our full dataset include the most commonly consumed items over the study period and over 80% of items in the diet at each site. To examine variation in nutritional composition, intake rates (energy and item), and availability among the same species/item combinations consumed at the two sites, matched Wilcoxon rank tests with continuity correction were used. Orangutans may consume several different items from the same species and thus for the matched species analyses we matched by food items. Because our goal was to compare the same individual food items found at each site, we did not use models with individual ID as a random effect as matched tests currently do not incorporate random effects. Thus, to reduce the potential effect of individual ID, we used feeding rates and energy intakes for adult females only for these matched items. Variation in fruit availability at the two sites was examined using T-tests matched by year and month.

To examine overall site differences in daily caloric intake, total feeding time, and feeding time on fruit, we used Generalized Additive Mixed Models (GAMM) in the lme4 packages of R v3.1.1 [86,87]. Fixed effects in the model included field site, sex/age class (independent nulliparous female, adult female (primiparous or multiparous), adult flanged male, adult unflanged male), and the percentage of fruiting trees. Orangutan identification was included as a random effect in each model. Total follow time or total feeding time was included as an offset function in the GAMM. In addition to the overall GAMMs, we further explored the data using GLMMs by breaking fruit availability into categories (high, middle, low; see above) to test if our results held during only the low fruit periods when we would expect the animals are most energetically stressed. All test results are reported as two-tailed and significance was set at α ≤ 0.05.

Results

The overall sampled diet in Tuanan was higher in lipids and total non-structural carbohydrates (TNC), while the diet in Sabangau was higher in neutral detergent fiber (NDF) (Fig 1a–1c; Table 1); there was no difference in crude protein between plants consumed at the two sites (Fig 1d, Table 1). This resulted in higher metabolizable energy (Kcal per 100g OM) and metabolizable energy per plant item (Kcal) at Tuanan (Fig 1e and 1f; Table 1).

thumbnail
Fig 1. Variation in macronutrient composition in the orangutan diets in Tuanan (T) and Sabangau (S).

All comparisons are based on organic matter (OM) and Wilcoxon Signed Rank Test were used. A significant negative Z-statistic indicates Tuanan is greater. (a) Lipids (Z = -2.17, p = 0.03); (b) Total non-structural carbohydrates (TNC; Z = -5.43, p < 0.0001); (c) Neutral detergent fiber (NDF; Z = 5.63, p < 0.0001); (d) Crude protein (CP; Z = 0.64, p = 0.52); (e) Metabolizable energy (Kcal/100 g OM) (Z = -5.55, p < 0.0001); (f) Metabolizable energy/item (Kcal)(Z = -2.64, p = 0.008). See Table 1 for complete statistical results.

http://dx.doi.org/10.1371/journal.pone.0138612.g001

thumbnail
Table 1. Variation in entire sampled diet in Sabangau (S) and Tuanan (T).

Wilcoxon Signed Rank Test were used to compare macronutrients and metabolizable energy (ME) (expressed as % OM) between the two sites. TNC = Total non-structural carbohydrates; CP = Crude Protein; NDF = Neutral Detergent Fiber; ME = metabolizable energy Means and standard errors along with sample size (n) are reported.

http://dx.doi.org/10.1371/journal.pone.0138612.t001

Comparison of the nutritional composition of 39 food items from 22 species that were consumed at both sites and for which matching data were available revealed that matched items in Tuanan were higher in crude protein and TNC, and lower in NDF; there was no difference in lipids among sites (Fig 2a–2d, Table 2). Metabolizable energy (Kcal per 100g OM) of matched items was higher at Tuanan compared to Sabangau, resulting in higher energy intake (Kcal/min) on these items (Fig 2e and 2f; Table 2). In other words, orangutans eating the same amount of a given food item receive higher energy intake at Tuanan compared to Sabangau. This higher energy intake was not due to differences in feeding rates or field dry weight (g) of these plant items (Table 2), and thus reflects the energy available in these matched items. The orangutans in Tuanan spent a greater percentage of their daily feeding time on these matched items compared to Sabangau orangutans (Fig 2g; Table 2), and this was not due to difference in stem density of these species (Fig 2h; Table 2).

thumbnail
Fig 2. Matched plant species comparisons of dietary items in Tuanan (T) and Sabangau (S).

All macronutrient and energy comparisons are based on organic matter (OM) and Matched Wilcoxon Rank Tests were used. A negative S-statistics indicates Tuanan is greater. (a) Crude protein (S = -207, p = 0.003); (b) TNC (S = -284, p < 0.0001); (c) NDF (S = 291, p < 0.0001); (d) Lipids (S = 109, p = 0.13); (e) Metabolizable energy (Kcal/100g OM)(S = -235, p = 0.0005; (f) Energy intake (Kcal/min) (S = 52.5, p = 0.049); (g) Percentage of time feeding on plant items (S = -106, p = 0.001). See Table 2 for complete statistical results.

http://dx.doi.org/10.1371/journal.pone.0138612.g002

thumbnail
Table 2. Variation in macronutrients, metabolizable energy (ME) (expressed as % OM), and measures of availability in matched plant items in Sabangau (S) and Tuanan (T).

Matched Wilcoxon Rank Tests were used to compare the two sites. TNC = Total non-structural carbohydrates; CP = Crude Protein; NDF = Neutral Detergent Fiber; ME = metabolizable energy. Means and standard errors along with sample size (n) are reported (n = 39 unless noted).

http://dx.doi.org/10.1371/journal.pone.0138612.t002

While these data clearly indicate that the nutritional quality of dietary items is greater in Tuanan, how this translates into daily energy intake is likely to have direct impacts on fitness. Daily caloric intake was significantly greater in Tuanan compared to Sabangau (Fig 3a; Table 3a). This was not due to the Tuanan orangutans spending more time feeding per day (Fig 3b; Table 3b); indeed, they actually spent less time feeding on fruit (Fig 3c, Table 3c). This pattern held during the low-fruit periods: Tuanan orangutans had greater caloric intake, but spent less time feeding on fruit compared to the Sabangau orangutans (Table 4). During the high-fruit periods, Tuanan orangutans consumed more energy and spent less time feeding, but they did not spend less time feeding on fruit as they did during the low fruit periods (Table 4).

thumbnail
Fig 3. Daily caloric intake (a), total feeding time (b), and fruit feeding time compared (c).

Site differences in (a) Daily caloric intake (t-statistic = 12.26, p < 0.0001), (b) Total feeding time (t-statistic = -6.35, p < 0.0001), and (c) Fruit feeding time (t-statistic = -7.19, p < 0.0001) between the two sites. T = Tuanan, S = Sabangau. Generalized additive mixed models (GAMM) were used. A positive t-statistic indicates Tuanan is higher. See Table 3 for models and full statistical results.

http://dx.doi.org/10.1371/journal.pone.0138612.g003

thumbnail
Table 3. Site variation in (a) Daily caloric intake, (b) Daily feeding time (min), and (c) Daily time spent feeding on fruit (min).

All models include the variable age/sex class: FLM = flanged male; NUF = nulliparous independent female; UFM = unflanged adult male; AF = adult female; Age/Sex class comparisons are against AF. FAI = Percentage of fruiting trees.

http://dx.doi.org/10.1371/journal.pone.0138612.t003

thumbnail
Table 4. Variation in daily energy intake (Kcal), daily feeding time (minute), and daily fruit feeding time (minutes) during low, medium, and high fruit periods.

GMM were used to compare the two sites and included orangutan ID as a random effect. Data represent mean ± SE.

http://dx.doi.org/10.1371/journal.pone.0138612.t004

Longer fruit feeding time in Sabangau was not a consequence of higher productivity, as fruit availability in Tuanan was marginally higher relative to Sabangau (Matched Paired t-test, t = 1.93, p = 0.05, df = 77; Fig 4; mean Tuanan = 4.92 ± 3.08, mean Sabangau = 4.54 ± 1.77). Although fruiting was correlated between the two sites (Spearman ρ = 0.58, p<0.0001), fluctuations in fruit availability were more extreme in Tuanan in both directions, with higher peaks (Wilcoxon Matched Sign Rank Test, Z = 3.84, p<0.0001, n = 11,12) and lower troughs of fruit availability in Tuanan (Wilcoxon Matched Sign Rank Test, Z = -3.84, p<0.0001, n = 10,11). However, the duration, in number of months, of the high and low fruit periods did not differ between the sites (Wilcoxon rank sums (high: Χ2 = 0.26, df = 1, p = 0.61; low Χ2 = 0.0045, df = 1, p = 0.95).

thumbnail
Fig 4. Percentage of fruiting trees over the entire study period in Tuanan (red) and Sabangau (blue).

http://dx.doi.org/10.1371/journal.pone.0138612.g004

Discussion

Overall, our predictions were supported: the plant items consumed by the orangutans in Tuanan were higher in nutritional quality, resulting in higher daily caloric intake. This result was consistent for both the overall diets consumed at both sites and for those items for which we had matched nutritional data. Orangutans in Sabangau spent a greater amount of time feeding on fruit, which has a higher energetic return compared to other items in their diet [28,29,52], but they still had lower daily energy intake compared to orangutans in Tuanan. Thus, it is likely that the Sabangau orangutans spend more time feeding on fruit, a resource with higher caloric gains per unit feeding time [85,88,89]), in an attempt to ‘make up for’ their typically lower quality diet [52]. In agreement with this, Harrison et al. [52] found no correlation between fruit availability, energy intake, and ketone production in the Sabangau orangutan population (with the exception of a fairly weak positive relationship between fruit availability and energy intake in flanged males, r2 = 0.162) and showed that these orangutans experienced prolonged periods of energy shortfalls. Conversely, in Tuanan, orangutans fall into a negative energy balance state during periods of low fruit availability when energy intake is lowest, as evidenced by significantly greater levels of ketone production, but not during high fruit periods [53]. During the low fruit period, Tuanan orangutans, on average, consumed 819 more calories per day compared to orangutan in Sabangau (Table 4). This difference was even more extreme during the high fruit periods, with Tuanan orangutans consuming 2345 more calories per day during the (Table 4). This may have severe consequences for the Sabangau orangutans: total daily energy expenditure exceeds energy intake during on average 84% of the months during the four years between 2003–2007 [52], whereas for Tuanan total daily energy expenditure exceeds energy intake for about 20% of the months [53,90]. Thus, during the high fruit periods, the Tuanan orangutans appear to be better able to build fat reserves that they can catabolize during the low fruit periods when they fall into a negative energy balance state. This places energy intake levels in Tuanan between Sabangau and Gunung Palung in West Kalimantan [29,52,88].

Differences in forest productivity in terms of overall fruit availability were not as apparent, although the peak fruit periods were higher in Tuanan, reaching up to 14% of stems sampled within a month compared to 9% at Sabangau. However, when fruit availability was low, it was also at lower levels in Tuanan. Thus, fruiting is more extreme in both directions in Tuanan. These differences are unlikely to be driven by climatic variation between the two sites, as rainfall and temperature comparisons revealed high similarities [68]. Harrison et al. [68] found significant variation in the onset of fruiting and flowering events both within and among species at the two sites, despite their close geographic proximity. Finally, other studies focusing on the relationship between nutrition and fruit availability have used the energy of fruits available/hectare as a measure of food availability [17,48,91]. We used FAI instead of this measure because this measure is more reliably consistent across researchers collecting phenology data at both sites and Harrison [85] found that FAI had a stronger effect on orangutan energy intake than did fruit-energy availability in Sabangau.

While both Tuanan and Sabangau are classified as peat-swamp forests, the ecological differences between the two sites, namely the shallower peat and a more alluvial flooding regime in Tuanan, likely contribute to the differences in plant nutrient availability and, hence, nutritional composition of orangutan foods, fruiting patterns, and overall fruit availability [see also 68]. Future studies should examine variation in mineral composition of the peat soils at the two sites and how these may be linked to this observed variation in plant nutritional quality.

The availability of fruit resources is considered a major factor in determining vertebrate frugivore densities and carrying capacities [11,15,16,92]. Recent studies have emphasized the value of examining the relationship between food availability and vertebrate population density on a small spatial scale, as ecological conditions are less likely to differ between neighboring populations in climatically similar areas, and thus any relationships that may exist are more likely to become apparent [11,93]. It is likely that the higher orangutan population density in Tuanan [56,69] is linked to higher nutritional quality of plant species and the resulting higher daily orangutan caloric intake observed in this study.

However, additional factors may also influence population density at the two sites. Both logging and particularly hunting have been demonstrated to affect orangutan population densities [12,14,55,56,94,95]. Tuanan and Sabangau both experienced legal and illegal logging disturbances prior to 2004 [58,69]. Although quantitative data on the intensity of these threats are not available, because Sabangau is closer to Central Kalimantan’s capital, Palangka Raya (11 km versus 58 km), it may have experienced higher intensities of logging and hunting. It is therefore probable that these historical processes, combined with lower food nutrient content and overall fruit availability, explain the lower orangutan population density in Sabangau.

A second line of evidence also supports a higher quality habitat in Tuanan relative to Sabangau: differences in orangutan home range characteristics. While overall adult female home range size does not appear to differ between Tuanan and Sabangau [9699], both overall home range and home range core areas (50% use) of females overlap more in Tuanan compared to Sabangau [97,99,100]. Specifically, related adult female home range overlap in Tuanan is 57% and core area overlap is 15%, compared to 38% and 0% overlap in Sabangau [97,100]. This suggests that, while adult females live at higher densities in Tuanan, they may experience less competition for nutrients, and thus can afford to have more overlapping home ranges. This finding concurs with a larger scale study that also found a positive relationship between primate density and home range overlap, which is expected in the absence of active territory defense [101].

The relatively solitary lifestyle, late weaning, and overall slow life history of orangutans is likely a consequence of the ecological conditions characteristic of Southeast Asian tropical forests [29,43,44,102,103] [; but see [104]]. These forests have overall low mean productivity and great inter-annual variation in productivity [3,57,105,106]. Currently, the data on comparative reproductive ecology of wild orangutans are few and sufficient data sets with complete inter-birth intervals from Sumatra and Borneo remain limited [see [47] for a review]. While we currently do not have a sufficient comparative sample with complete IBIs and reproductive rates from the two field sites, it will be interesting to test if reproductive rates and ultimately fitness are higher in Tuanan compared to Sabangau as our sample size increases with future observations.

Conclusions

In summary, our data support a link between bottom-up regulatory factors, variation in nutritional intake of a mostly frugivorous mammal species, and population density. This study has implications for the conservation of viable habitat for endangered frugivores like orangutans. Peat-swamp forests hold the largest remaining relatively undisturbed populations of Bornean orangutans (Pongo pygmaeus) and are considered excellent habitats for orangutans [56,58,60]. As more orangutans are relocated due to agricultural pressures, specifically the growing pressures of oil palm expansion in peatland habitats [107,108], finding suitable habitats that provide sufficient energy for orangutans has become an increasing challenge [109]. Here, we have shown that what appears to be similar habitat does not necessarily translate into similar nutrient intake of its inhabitants. Our results indicate that reductions in habitat quality that would be expected following human disturbance, and consequently the availability of higher-quality fruits, are likely to lead to negative impacts on orangutan nutrition, with potential long-term impacts on population density. This suggests that it is important to incorporate careful habitat quality assessment and maintenance into future conservation action plans for this endangered species.

Supporting Information

S1 Fig. Map of Tuanan Orangutan Research Project area and the Sabangau Study area, Natural Laboratory of Peat-swamp Forest (NLPSF).

Reprinted from [68] under a CC BY license, with permission from the Assoc. for Tropical Biology and Conservation original copyright 2015.

doi:10.1371/journal.pone.0138612.s001

(PDF)

S1 Table. Breakdown of the number of individuals in each sex class in this study.

doi:10.1371/journal.pone.0138612.s002

(PDF)

S2 Table. Site variation in daily caloric intake (using the high NDF coefficient of 1.6); FLM = flanged male; NUF = nulliparous independent female; UFM = unflanged adult male; AF = adult female; Age/Sex class comparisons are against AF.

FAI = Percentage of fruiting trees.

doi:10.1371/journal.pone.0138612.s003

(PDF)

Acknowledgments

We thank the Tuanan team of assistants, staff, and all of the students for their efforts in data collection, Tatang Mitra Setia, Carel van Schaik, Fakultas Biologi Universitas Nasional (UNAS) in Jakarta for their partnership and support; and in Sabangau, Suwido Limin and CIMTROP, plus all of the numerous staff, students and volunteers who assisted with data collection. We gratefully acknowledge the Indonesian State Ministry for Research and Technology (RISTEK), the Indonesian Institute of Science (LIPI), the Centre for the International Cooperation in Sustainable Management of Tropical Peatlands (CIMTROP) at the University of Palangka Raya, the Director General Departemen Kehutanan (PHKA), Departamen Dalam Negri, the BKSDA Palangkaraya, the local government in Central Kalimantan, the Bornean Orangutan Survival Foundation (BOSF-Indonesia) and Mawas in Palangkaraya for their permission and support to the project.

Author Contributions

Conceived and designed the experiments: ERV MEH WRF. Performed the experiments: ERV MEH AZ SS TF WRF HMB. Analyzed the data: ERV TDB SEA. Contributed reagents/materials/analysis tools: ERV MEH SH HMB MAN WRF SSU. Wrote the paper: ERV MEH HMB SH MAN WRF SSU.

References

  1. 1. Oates JF, Whitesides GH, Davies AG, Waterman PG, Green SM, et al. (1990) Determinants of variation in tropical forest primate biomass—new evidence from West Africa. Ecology 71: 328–343. doi: 10.2307/1940272
  2. 2. Bourliere F (1985) Primate communities—their structure and role in tropical ecosystems. International Journal of Primatology 6: 1–26. doi: 10.1007/bf02693694
  3. 3. Wich SA, Vogel ER, Larsen MD, Fredriksson G, Leighton M, et al. (2011) Forest fruit production is higher on Sumatra than on Borneo. Plos One 6. doi: 10.1371/journal.pone.0021278
  4. 4. Sinclair ARE, Krebs CJ (2002) Complex numerical responses to top-down and bottom-up processes in vertebrate populations. Philosophical Transactions: Biological Sciences 357: 1221–1231. doi: 10.1098/rstb.2002.1123
  5. 5. Vucetich JA, Peterson RO (2004) The influence of top–down, bottom–up and abiotic factors on the moose (Alces alces) population of Isle Royale. Proceedings of the Royal Society London B 271: 183–189. doi: 10.1098/rspb.2003.2589
  6. 6. DeGabriel JL, Moore BD, Felton AM, Ganzhorn JU, Stolter C, et al. (2014) Translating nutritional ecology from the laboratory to the field: milestones in linking plant chemistry to population regulation in mammalian browsers. Oikos 123: 298–308. doi: 10.1111/j.1600-0706.2013.00727.x
  7. 7. Sharp A, McCallum H (2014) Bottom-up processes in a declining yellow-footed rock-wallaby (Petrogale xanthopus celeris) population. Austral Ecology: doi: 10.1111/aec.12185.
  8. 8. Kay RF, Madden RH, van Schaik C, Higdon D (1997) Primate species richness is determined by plant productivity: Implications for conservation. Proceedings of the National Academy of Sciences of the United States of America 94: 13023–13027. pmid:9371793 doi: 10.1073/pnas.94.24.13023
  9. 9. Ganzhorn JU (1992) Leaf chemistry and the biomass of folivorous primates in tropical forests—test of a hypothesis. Oecologia 91: 540–547. doi: 10.1007/bf00650329
  10. 10. Hanya G, Stevenson P, van Noordwijk M, Wong ST, Kanamori T, et al. (2011) Seasonality in fruit availability affects frugivorous primate biomass and species richness. Ecography 34: 1009–1017. doi: 10.1111/j.1600-0587.2010.06775.x
  11. 11. Chapman CA, Chapman LJ (1999) Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys. Primates 40: 215–231. doi: 10.1007/BF02557712. pmid:23179542
  12. 12. Felton AM, Engstrom LM, Felton A, Knott CD (2003) Orangutan population density, forest structure and fruit availability in hand-logged and unlogged peat swamp forests in West Kalimantan, Indonesia. Biological Conservation 114: 91–101. doi: 10.1016/s0006-3207(03)00013-2
  13. 13. Potts KB, Chapman CA, Lwanga JS (2009) Floristic heterogeneity between forested sites in Kibale National Park, Uganda: insights into the fine-scale determinants of density in a large-bodied frugivorous primate. Journal of Animal Ecology 78: 1269–1277. doi: 10.1111/j.1365-2656.2009.01578.x. pmid:19523110
  14. 14. Wich S, Buij R, van Schaik C (2004) Determinants of orangutan density in the dryland forests of the Leuser Ecosystem. Primates 45: 177–182. pmid:15098098 doi: 10.1007/s10329-004-0080-1
  15. 15. Marshall AJ, Leighton M (2006) How does food availability limit the population density of white-bearded gibbons? In: Hohmann G RM, Boesch C, editor. Feeding Ecology of the Apes and other Primates. Cambridge: Cambridge University Press. pp. 311–333.
  16. 16. Marshall A, Beaudrot L, Wittmer H (2014) Responses of primates and other frugivorous vertebrates to plant resource variability over space and time at Gunung Palung National Park. International Journal of Primatology 35: 1178–1201. doi: 10.1007/s10764-014-9774-4
  17. 17. Wright E, Grueter CC, Seiler N, Abavandimwe D, Stoinski TS, et al. (2015) Energetic responses to variation in food availability in the two mountain gorilla populations (Gorilla beringei beringei). American Journal of Physical Anthropology Early View Online: n/a-n/a. doi: 10.1002/ajpa.22808
  18. 18. Rothman JM, Plumptre AJ, Dierenfeld ES, Pell AN (2007) Nutritional composition of the diet of the gorilla (Gorilla beringei): a comparison between two montane habitats. Journal of Tropical Ecology 23: 673–682. doi: 10.1017/s0266467407004555
  19. 19. Chapman CA, Chapman LJ, Bjorndal KA, Onderdonk DA (2002) Application of protein-to-fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology 23: 283–310.
  20. 20. Chapman CA, Chapman LJ, Naughton-Treves L, Lawes MJ, McDowell LR (2004) Predicting folivorous primate abundance: Validation of a nutritional model. American Journal of Primatology 62: 55–69. pmid:14983464 doi: 10.1002/ajp.20006
  21. 21. Wasserman MD, Chapman CA (2003) Determinants of colobine monkey abundance: the importance of food energy, protein and fibre content. Journal of Animal Ecology 72: 650–659. doi: 10.1046/j.1365-2656.2003.00736.x
  22. 22. Wallis IR, Edwards MJ, Windley H, Krockenberger AK, Felton A, et al. (2012) Food for folivores: nutritional explanations linking diets to population density. Oecologia 169: 281–291. doi: 10.1007/s00442-011-2212-9. pmid:22246432
  23. 23. Fashing PJ, Dierenfeld ES, Mowry CB (2007) Influence of plant and soil chemistry on food selection, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. International Journal of Primatology 28: 673–703. doi: 10.1007/s10764-006-9096-2
  24. 24. Ganzhorn JU, Arrigo-Nelson S, Boinski S, Bollen A, Carrai V, et al. (2009) Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PLoS One 4. doi: 10.1371/journal.pone.0008458.
  25. 25. Rode KD, Chapman CA, McDowell LR, Stickler C (2006) Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus ascanius). Biotropica 38: 625–634. doi: 10.1111/j.1744-7429.2006.00183.x
  26. 26. Hawes JE, Peres CA (2014) Ecological correlates of trophic status and frugivory in neotropical primates. Oikos 123: 365–377. doi: 10.1111/j.1600-0706.2013.00745.x
  27. 27. Milton K (2004) Ferment in the family tree: Does a frugivorous dietary heritage influence contemporary patterns of human ethanol use? Integrative and Comparative Biology 44: 304–314. doi: 10.1093/icb/44.4.304. pmid:21676714
  28. 28. Conklin-Brittain NL, Knott CD, Wrangham RW (2006) Energy intake by wild chimpanzees and orangutans: methodological considerations and a preliminary comparison. In: Hohmann G, Robbins M, Boesch C, editors. Feeding ecology in apes and other primates: ecological, physiological and behavioural aspects. Cambridge: Cambridge University Press. pp. 445–471.
  29. 29. Knott CD (1998) Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. International Journal of Primatology 19: 1061–1079.
  30. 30. Rothman JM, Raubenheimer D, Chapman CA (2011) Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein. Biology Letters 7: 847–849. doi: 10.1098/rsbl.2011.0321. pmid:21632622
  31. 31. Marshall AJ, Boyko CM, Feilen KL, Boyko RH, Leighton M (2009) Defining fallback foods and assessing their importance in primate ecology and evolution. American Journal of Physical Anthropology 140: 603–614. doi: 10.1002/ajpa.21082. pmid:19890868
  32. 32. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B, editor. Sexual selection and the descent of man. Chicago: Aldine. pp. 136–179.
  33. 33. Gadgil M, Bossert WH (1970) Life historical consequences of natural selection. American Naturalist 104: 1–24. doi: 10.1086/282637
  34. 34. Schneider JE, Wade GN (2000) Inhibition of reproduction in ser-vice of energy balance. In: Wallen K, Schneider JE, editors. Reproduction in Context: Social and Environ-mental Influences on Reproduction. Cambridge, Massachusettes: MIT Press. pp. 35–82.
  35. 35. van Noordwijk MA, van Schaik CP (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40: 105–130. doi: 10.1007/BF02557705. pmid:23179535
  36. 36. Altmann J, Alberts SC (2003) Variability in reproductive success viewed from a life-history perspective in baboons. American Journal of Human Biology 15: 401–409. pmid:12704715 doi: 10.1002/ajhb.10157
  37. 37. Borries C, Koenig A, Winkler P (2001) Variation of life history traits and mating patterns in female langur monkeys (Semnopithecus entellus). Behavioral Ecology and Sociobiology 50: 391–402. doi: 10.1007/s002650100391
  38. 38. Potts KB (2013) Nutritional ecology and reproductive output in female chimpanzees (Pan troglodytes): variation among and within populations. In: Clancy KBH, Hinde K, Rutherford JN, editors. Building Babies: Primate Development in Proximate and Ultimate Perspective: Springer New York. pp. 83–100.
  39. 39. Pusey A, Williams J, Goodal J (1997) The influence of dominance rank on the reproductive success of female chimpanzees. Science 277: 828–831. pmid:9242614 doi: 10.1126/science.277.5327.828
  40. 40. Emery Thompson M, Kahlenberg SM, Gilby IC, Wrangham RW (2007) Core area quality is associated with variance in reproductive success among female chimpanzees at Kibale National Park. Animal Behaviour 73: 501–512. doi: 10.1016/j.anbehav.2006.09.007
  41. 41. Thompson ME, Wrangham RW (2008) Diet and reproductive function in wild female chimpanzees (Pan troglodytes schweinfurthii) at Kibale National Park, Uganda. American Journal of Physical Anthropology 135: 171–181. pmid:18046778 doi: 10.1002/ajpa.20718
  42. 42. Kuze N, Dellatore D, Banes GL, Pratje P, Tajima T, et al. (2012) Factors affecting reproduction in rehabilitant female orangutans: young age at first birth and short inter-birth interval. Primates 53: 181–192. doi: 10.1007/s10329-011-0285-z. pmid:22109351
  43. 43. van Noordwijk MA, Willems EP, Atmoko SSU, Kuzawa CW, van Schaik CP (2013) Multi-year lactation and its consequences in Bornean orangutans (Pongo pygmaeus wurmbii). Behavioral Ecology and Sociobiology 67: 805–814. doi: 10.1007/s00265-013-1504-y
  44. 44. Knott C (2001) Female reproductive ecology in apes. In: Ellison PT, editor. Reproductive Ecology and Human Evolution. Hawthorne, New York: Aldine De Gruyter. pp. 429–463.
  45. 45. Galdikas BMF, Wood JW (1990) Birth spacing patterns in humans and apes. American Journal of Physical Anthropology 83: 185–191. pmid:2248378 doi: 10.1002/ajpa.1330830207
  46. 46. Wich SA, Utami-Atmoko SS, Setia TM, Rijksen HD, Schurmann C, et al. (2004) Life history of wild Sumatran orangutans (Pongo abelii). Journal of Human Evolution 47: 385–398. pmid:15566945 doi: 10.1016/j.jhevol.2004.08.006
  47. 47. Knott CD, Emery Thompson M, Wich SA (2009) The ecology of female reproduction in wild orangutans. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP, editors. Orangutans: geographic variation in behavioral ecology and conservation. New York: Oxford University Press. pp. 171–188.
  48. 48. Knott CD (2005) Energetic responses to food availability in the great apes: inplications for hominin evolution. In: Brockman DK, van Schaik CP, editors. Seasonality in Primates: studies of living and extinct human and non-human primates. New York: Cambridge University Press. pp. 351–378.
  49. 49. Vogel ER, Knott CD, Crowley BE, Blakely MD, Larsen MD, et al. (2012) Bornean orangutans on the brink of protein bankruptcy. Biology Letters 8: 333–336. doi: 10.1098/rsbl.2011.1040. pmid:22171019
  50. 50. Morrogh-Bernard HC, Husson SJ, Knott CD, Wich SA, van Schaik CP, et al. (2009) Orangutan activity budgets and diet: a comparison between species, populations and habitats. In: Wich SA, Utami Atmoko S, Mitra Setia T, van Schaik CP, editors. Orangutans: Geographic Variation in Behavioral Ecology and Conservation. New York: Oxford University Press. pp. 119–133.
  51. 51. Russon AE, Wich SA, Ancrenaz M, Kanamori T, Knott CD, et al. (2009) Geographic variation in orangutan diets. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP, editors. Orangutans: Geographic Variation in Behavioral Ecology. Oxford: Oxford University Press. pp. 135–156.
  52. 52. Harrison ME, Morrogh-Bernard HC, Chivers DJ (2010) Orangutan energetics and the influence of fruit availability in the nonmasting peat-swamp forest of Sabangau, Indonesian Borneo. International Journal of Primatology 31: 585–607. doi: 10.1007/s10764-010-9415-5
  53. 53. Vogel ER, Bransford TD, Moldawer AM, Van Noordwijk MA, Atmoko SSU, et al. (2014) Do Bornean orangutans (Pongo pygmaeus wurmbii) in a peat-swamp habitat experience energetic stress during periods of fruit scarcity? American Journal of Physical Anthropology 153: 262–262.
  54. 54. Delgado RA, van Schaik CP (2000) The behavioral ecology and conservation of the orangutan (Pongo pygmaeus): A tale of two islands. Evolutionary Anthropology 9: 201–218. doi: 10.1002/1520-6505(2000)9:5<201::aid-evan2>3.0.co;2-y
  55. 55. Meijaard E, Buchori D, Hadiprakarsa Y, Utami-Atmoko SS, Nurcahyo A, et al. (2011) Quantifying killing of orangutans and human-orangutan conflict in Kalimantan, Indonesia. Plos One 6. doi: 10.1371/journal.pone.0027491
  56. 56. Husson SJ, Wich SA, Marshall AJ, Dennis RD, Ancrenaz M, et al. (2009) Orangutan distribution, density, abundance and impacts of disturbance. In: Wich SA, Utami Atmoko S, Mitra Setia T, van Schaik CP, editors. Orangutans: Geographic Variation in Behavioral Ecology and Conservation. New York: Oxford University Press. pp. 77–96.
  57. 57. Marshall AJ, Ancrenaz M, Brearly FQ, Fredriksson GM, Ghaffar N, et al. (2009) The effects of forest phenology and floristics on populations of Bornean and Sumatran orangutans: Are Sumatran forests better orangutan habitats than Bornean forests? In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP, editors. Orangutans: Geographic Variation in Behavioral Ecology and Conservation. Oxford: Oxford University Press. pp. 97–117.
  58. 58. Morrogh-Bernard H, Husson S, Page SE, Rieley JO (2003) Population status of the Bornean orang-utan (Pongo pygmaeus) in the Sebangau peat swamp forest, Central Kalimantan, Indonesia. Biological Conservation 110: 141–152. doi: 10.1016/s0006-3207(02)00186-6
  59. 59. Ancrenaz M (2007) Orangutan aerial survey in Sebangau National Park, Central Kalimantan Indonesia, Sebangau Project, Kalimantan Tengah, WWF Indonesia. 1–40 p.
  60. 60. Wich SA, Meijaard E, Marshall AJ, Husson S, Ancrenaz M, et al. (2008) Distribution and conservation status of the orang-utan (Pongo spp.) on Borneo and Sumatra: how many remain? Oryx 42: 329–339. doi: 10.1017/s003060530800197x
  61. 61. Cannon CH, Curran LM, Marshall AJ, Leighton M (2007) Beyond mast-fruiting events: Community asynchrony and individual dormancy dominate woody plant reproductive behavior across seven Bornean forest types. Current Science 93: 1558–1566.
  62. 62. Page SE, Rieley JO, Shotyk ØW, Weiss D (1999) Interdependence of peat and vegetation in a tropical peat swamp forest. Philosophical Transactions of the Royal Society B-Biological Sciences 354: 1885–1897. doi: 10.1098/rstb.1999.0529
  63. 63. Sulistiyanto Y, Rieley J, Limin S. Nutrient dynamics in different sub-types of ombrotrophic peat swamp forest in Central Kalimantan, Indonesia. In: Päivänen J, editor; 2004; Tampere, Finland.
  64. 64. Page SE, Rieley JO, Doody S, Hodgson S, Husson S, et al. (1997) Biodiversity of tropical peat swamp forest: A case study of animal diversity in the Sungai Sebangau Catchment of Central Kalimantan, Indonesia. In: Page SE, Rieley JO, editors. Biodiversity and Sustainability of Tropical Peatlands. Cardigan: Samara Publishing Limited. pp. 231–242.
  65. 65. Page SE, Rieley JO, Banks CJ (2011) Global and regional importance of the tropical peatland carbon pool. Global Change Biology 17: 798–818. doi: 10.1111/j.1365-2486.2010.02279.x
  66. 66. Wich SA, Utami Atmoko S, Mitra Setia T, van Schaik CP (2009) Preface. Orangutans: Geographic Variation in Behavioral Ecology and Conservation. New York: Oxford University Press. pp. xix–xxxi.
  67. 67. Thomas L (2002) Coal Geology. West Sussex, England: John Wiley & Sons Ltd.
  68. 68. Harrison ME, Zweifel N, Husson SJ, Cheyne SM, D'arcy LD, et al. (In press) Disparity in onset timing and frequency of flowering and fruiting events in two Bornean peat-swamp forests. Biotropica. doi: 10.1111/btp.12265
  69. 69. van Schaik CP, Wich SA, Utami SS, Odom K (2005) A simple alternative to line transects of nests for estimating orangutan densities. Primates 46: 249–254. pmid:15983724 doi: 10.1007/s10329-005-0134-z
  70. 70. Alavi SE (unpublished data).
  71. 71. Harrison ME, Husson SJ, Zweifel N, D’arcy LJ, Morrogh-Bernard HC, et al. (2010) The fruiting phenology of peat-swamp forest tree species at Sabangau and Tuanan, Central Kalimantan, Indonesia.
  72. 72. Harrison ME, Vogel ER, Morrogh-Bernard HC, van Noordwijk MA (2009) Methods for calculating activity budgets compared: A case study using orangutans. American Journal of Primatology 71: 353–358. doi: 10.1002/ajp.20655. pmid:19065642
  73. 73. van Schaik CP (1999) The socioecology of fission-fusion sociality in orangutans. Primates 40: 73–90. doi: 10.1007/bf02557703
  74. 74. Nater A, Nietlisbach P, Arora N, van Schaik CP, van Noordwijk MA, et al. (2011) Sex-biased dispersal and volcanic activities shaped phylogeographic patterns of extant orangutans (genus: Pongo). Molecular Biology and Evolution 28: 2275–2288. doi: 10.1093/molbev/msr042. pmid:21335339
  75. 75. Arora N, Nater A, van Schaik CP, Willems EP, van Noordwijk MA, et al. (2010) Effects of Pleistocene glaciations and rivers on the population structure of Bornean orangutans (Pongo pygmaeus). Proceedings of the National Academy of Sciences of the United States of America 107: 21376–21381. doi: 10.1073/pnas.1010169107. pmid:21098261
  76. 76. Vogel ER, van Woerden JT, Lucas PW, Atmoko SSU, van Schaik CP, et al. (2008) Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes schweinfurthii and Pongo pygmaeus wurmbii. Journal of Human Evolution 55: 60–74. doi: 10.1016/j.jhevol.2007.12.005. pmid:18243275
  77. 77. Chapman CA, Chapman LJ, Rode KD, Hauck EM, McDowell LR (2003) Variation in the nutritional value of primate foods: Among trees, time periods, and areas. International Journal of Primatology 24: 317–333. doi: 10.1023/a:1023049200150
  78. 78. Pierce WC, Haenisch EL (1947) Quantitative Analysis. London: John Wiley & Sons, INc.
  79. 79. (Foss Analytical Manual, 2003) Manual for Kjeltec System 2300 Distilling and Titration Unit.
  80. 80. Goering HK, van Soest PJ (1970) Forage fiber analysis. In: ARS , editor. Agricultural Handbook, No 379. Washington, DC: U.S.D.A.
  81. 81. Robertson JB, van Soest PJ (1980) The analysis of dietary fiber in food. In: James WPT, Theander O, editors. The detergent system of analysis and its application to human foods. New York: Marcel Dekker, Inc. pp. 123–158.
  82. 82. Oyarzun SE, Crawshaw GJ, Valdes EV (1996) Nutrition of the tamandua: I. nutrient composition of termites (Nasutitermes spp.) and stomach contents from wild tamanduas (Tamandua tetradactyla). Zoo Biology 15: 509–524. doi: 10.1002/(sici)1098-2361(1996)15:5<509::aid-zoo7>3.0.co;2-f
  83. 83. O'Malley RC, Power ML (2014) The energetic and nutritional yields from insectivory for Kasekela chimpanzees. Journal of Human Evolution 71: 46–58. doi: 10.1016/j.jhevol.2013.09.014. pmid:24698197
  84. 84. Milton K, Demment MW (1988) Digestion and passage kinetics of chimpanzees fed high and low-fiber diets and comparison with human data. Journal of Nutrition 118: 1082–1088. pmid:2843616
  85. 85. Harrison ME (2009) Orang-utan feeding behaviour in Sabangau, Central Kalimantan [Doctoral]. Cambridge: University of Cambridge.
  86. 86. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, et al. (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24: 127–135. doi: 10.1016/j.tree.2008.10.008
  87. 87. R Developement Core Team (2015) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
  88. 88. Knott CD (1999) Reproductive, physiological and behavioral responses of orangutans in Borneo to fluctuations in food availability [PhD]. Boston, Massachusetts: Harvard University.
  89. 89. Vogel ER (unpublished data).
  90. 90. Vogel ER, Alavi SE, Utami Atmoko SS, Erb WM, van Noordwijk MA, et al. (in prep.) Nutritional ecology of wild Bornean orangutans (Pongo pygmaeus wurmbii) in a peat swamp habitat: consequences of age, sex, and season.
  91. 91. Emery Thompson M, Knott CD (2008) Urinary C-peptide of insulin as a non-invasive marker of energy balance in wild orangutans. Horm Behav 53: 526–535. doi: 10.1016/j.yhbeh.2007.12.005. pmid:18255067
  92. 92. Curran LM, Leighton M (2000) Vertebrate responses to spatiotemporal variation in seed production of mast-fruiting Dipterocarpaceae. Ecological Monographs 70: 101–128. doi: 10.2307/2657169
  93. 93. Chapman CA, Struhsaker TT, Skorupa JP, Snaith TV, Rothman JM (2010) Understanding long-term primate community dynamics: implications of forest change. Ecological Applications 20: 179–191. pmid:20349839 doi: 10.1890/09-0128.1
  94. 94. Marshall AJ, Nardiyono , Engstrom LM, Pamungkas B, Palapa J, et al. (2006) The blowgun is mightier than the chainsaw in determining population density of Bornean orangutans (Pongo pygmaeus morio) in the forests of East Kalimantan. Biol Conserv 129: 566–578. doi: 10.1016/j.biocon.2005.11.025
  95. 95. Meijaard E, Wich S (2007) Putting orang-utan population trends into perspective. Current Biology 17: R540–R540. pmid:17637350 doi: 10.1016/j.cub.2007.05.016
  96. 96. Singleton I, Knott CD, Morrogh-Bernard HC, Wich SA, van Schaik CP (2009) Ranging behavior of orangutan females and social organization. In: Wich SA, Utami Atmoko SS, Mitra Setia T, van Schaik CP, editors. Orangutans: Geographic variation in Behavioral Ecology and Conservation. Oxford: Oxford University Press. pp. 205–212.
  97. 97. van Noordwijk MA, Arora N, Willems EP, Dunkel LP, Amda RN, et al. (2012) Female philopatry and its social benefits among Bornean orangutans. Behavioral Ecology and Sociobiology 66: 823–834. doi: 10.1007/s00265-012-1330-7
  98. 98. Wartmann FM, Purves RS, van Schaik CP (2010) Modelling ranging behaviour of female orang-utans: a case study in Tuanan, Central Kalimantan, Indonesia. Primates 51: 119–130. doi: 10.1007/s10329-009-0186-6. pmid:20127138
  99. 99. Morrogh-Bernard H (2009) Orang-utan behavioral ecology in the Sabangau peat-swamp forest, Borneo [Doctor of Philosophy]. Cambridge: University of Cabmbridge. 1–290 p.
  100. 100. Morrogh-Bernard H (unpublished data).
  101. 101. Pearce F, Carbone C, Cowlishaw G, Isaac NJB (2013) Space-use scaling and home range overlap in primates. doi: 10.1098/rspb.2012.2122
  102. 102. Jaeggi AV, Dunkel LP, Van Noordwijk MA, Wich SA, Sura AAL, et al. (2010) Social learning of diet and foraging skills by wild immature bornean orangutans: implications for culture. American Journal of Primatology 72: 62–71. doi: 10.1002/ajp.20752. pmid:19790189
  103. 103. van Noordwijk MA, van Schaik CP (2005) Development of ecological competence in Sumatran orangutans. American Journal of Physical Anthropology 127: 79–94. pmid:15472890 doi: 10.1002/ajpa.10426
  104. 104. Anderson HB, Thompson ME, Knott CD, Perlins L (2008) Fertility and mortality patterns of captive Bornean and Sumatran orangutans: Is there a species difference in life history? Journal of Human Evolution 54: 34–42. pmid:17804037 doi: 10.1016/j.jhevol.2007.05.014
  105. 105. Terborgh J, van Schaik CP (1987) Convergence vs. non-convergence in primate communities. In: Gee JHR, Giller PS, editors. Organization of Communities: Past and Present. Oxford: Blackwell Scientific Publications. pp. 205–226.
  106. 106. van Schaik CP, Pfannes KR (2005) Tropical climates and phenology: a primate perspective. In: Brockman DK, van Schaik CP, editors. Seasonality in primates: Studies of living and extinct human and non-human primates. New York: Cambridge Univ Press. pp. 23–54.
  107. 107. Venter O, Meijaard E, Wilson K (2008) Strategies and alliances needed to protect forest from palm-oil industry. Nature 451: 16–16. doi: 10.1038/451016a. pmid:18172476
  108. 108. Nantha HS, Tisdell C (2009) The orangutan-oil palm conflict: economic constraints and opportunities for conservation. Biodiversity and Conservation 18: 487–502. doi: 10.1007/s10531-008-9512-3
  109. 109. Russon AE (2009) Orangutan Rehabilitation and Reintroduction. In: Wich S, Utami SS, Mitra-Setia T, van Schaik CP, editors. Orangutans: Geographic Variation in Behavioral Ecology and Conservation. Oxford: Oxford University Press. pp. 327–350.