International Journal of Primatology

, Volume 38, Issue 2, pp 122–150

Nutritional Characteristics of Wild and Cultivated Foods for Chimpanzees (Pan troglodytes) in Agricultural Landscapes

Article

Abstract

Primate habitats are being transformed by human activities such as agriculture. Many wild primates include cultivated foods (crops) in their diets, calling for an improved understanding of the costs and benefits of crop feeding. We measured the macronutrient and antifeedant content of 44 wild and 21 crop foods eaten by chimpanzees (Pan troglodytes schweinfurthii) in a mosaic habitat at Bulindi, Uganda, to evaluate the common assertion that crops offer high nutritional returns compared to wild forage for primates. In addition, we analyzed 13 crops not eaten at Bulindi but that are consumed by chimpanzees elsewhere to assess whether nutritional aspects explain why chimpanzees in Bulindi ignored them. Our analysis of their wild plant diet (fruit, leaves, and pith) corresponds with previous chemical analyses of primate plant foods. Compared to wild food equivalents, crops eaten by the chimpanzees contained higher levels of digestible carbohydrates (mainly sugars) coupled with lower amounts of insoluble fiber and antifeedants. Cultivated fruits were relatively nutritious throughout the ripening process. Our data support the assumption that eating cultivated foods confers energetic advantages for primates, although crops in our sample were low in protein and lipids compared to some wild foods. We found little evidence that crops ignored by the chimpanzees were less nutritious than those that they did eat. Nonnutritional factors, e.g., similarity to wild foods, probably also influence crop selection. Whether cultivated habitats can support threatened but flexible primates such as chimpanzees in the long term hinges on local people’s willingness to share their landscape and resources with them.

Keywords

Agroecosystems Crop foraging Cultivars Dietary flexibility Human-dominated landscapes Nutritional ecology 

Introduction

Conversion of forests for subsistence and commercial agriculture is continuing apace throughout the world’s most biodiverse regions (Gibbs et al. 2010; Laurance et al. 2014; Tilman et al. 2001). While agricultural expansion erodes wild foods, ecologically and behaviorally flexible species may exploit these new environments and their novel foods (McLennan and Hockings 2014). Crop feeding by wildlife (commonly termed crop raiding) receives considerable attention because it can cause conservation conflicts through impacts on local livelihoods (Conover 2002; Hill 1997; MacKenzie and Ahabyona 2012; Redpath et al. 2013). Understanding the attractiveness of crops, i.e., cultivated foods, to wildlife thus has strong relevance for conservation management (Dostaler et al. 2011; Osborn 2004; Rode et al. 2006).

Nonhuman primates (hereafter primates) feature prominently in the literature on crop damage by wild tropical vertebrates (Paterson and Wallis 2005). The propensity of generalist primate foragers to exploit areas of human settlement and cultivation is well documented, e.g., members of Macaca, Papio, and Chlorocebus in Asia and Africa (Brennan et al. 1985; Hill 2000; Priston and McLennan 2013; Strum 2010), and Alouatta, Cebus, and Sapajus in the Neotropics (Bicca-Marques and Calegaro-Marques 1994; McKinney 2011; Spagnoletti et al. 2017). However, with the expansion of agroecosystems in primate habitats a broad range of other taxa have been found to eat crops (Estrada et al. 2012). These include species not usually regarded as generalist, omnivorous feeders, e.g., Trachypithecus vetulus (Nijman 2012), Procolobus kirkii (Nowak and Lee 2013), and Gorilla beringei beringei (Seiler and Robbins 2016), suggesting that more “specialist” primates can also respond flexibly to agricultural encroachment, albeit if only in the short term (Nowak and Lee 2013).

Humans have selected agricultural foods to be easily digestible, energy rich, and low in plant secondary compounds that impede digestion or include harmful toxins (Milton 1999). Including crops in the diet has far-reaching consequences for primates. Frequent crop consumption is associated with major changes in activity budgets, with primates typically spending more time resting and in social behavior and less time traveling and foraging, apparently due to energetic benefits of crops that allow metabolic demands to be met sooner, e.g., Papio cynocephalus (Altmann and Muruthi 1988), P. anubis (Eley et al. 1989; Strum 2010; Warren et al. 2011), and Chlorocebus aethiops (Saj et al. 1999). Crop feeding has further been linked to reduced physiological stress (P. anubis: Lodge et al. 2013) and possibly enhanced immune responses (Colobus guereza: Chapman et al. 2006; P. anubis: Eley et al. 1989; Weyher et al. 2006). Despite significant costs, i.e., injury or mortality from pest management, frequent crop consumption may confer life history and reproductive advantages to primates, e.g., improved body condition and increased adult weight, reduced infant mortality, shorter interbirth intervals, and earlier reproductive onset (Macaca fuscata: Sugiyama and Ohsawa 1982; P. anubis: Lodge et al. 2013; Strum 2010; Warren et al. 2011). Even so, elevated serum insulin and cholesterol levels in refuse foraging P. anubis and P. cynocephalus have been reported (Kemnitz et al. 2002).

High nutritional returns of crops compared to wild forage are usually assumed. Few studies have quantified nutritional characteristics of both wild and cultivated foods in diets of crop foraging primates. In one study, cultivated cacao (cocoa) eaten by Macaca tonkeana was higher in digestible carbohydrates and lower in insoluble fiber compared to wild fruits in their diet (Riley et al. 2013). Similarly, maize and potato eaten by Papio anubis had markedly lower insoluble fiber and thus greater digestibility compared to many of their wild plant foods (Forthman-Quick and Demment 1988).

Chimpanzees (Pan troglodytes) offer a useful model for examining nutritional attributes of “natural” vs. cultivated foods in diets of wild primates. Although varying by habitat and season, their natural diets are consistently dominated by ripe fruits that they seek out even when scarce, leading some authors to label them ripe fruit specialists (Ghiglieri 1984; Watts et al. 2012; Wrangham et al. 1998). In general, chimpanzee food selection reflects a preference for higher levels of macronutrients, particularly easily digestible sugars, and lower amounts of insoluble fiber and digestion-inhibiting antifeedants, i.e., polyphenols and condensed tannins, which characterize ripe fruit (Hohmann et al. 2010; Matsumoto-Oda and Hayashi 1999; Remis 2002; Reynolds et al. 1998; Sommer et al. 2011; Wrangham et al. 1998). Unripe fruits may be eaten but are usually lower in sugar and higher in fiber and antifeedants than ripe ones (Houle et al. 2014; Wrangham and Waterman 1983), although chimpanzees seem to tolerate moderate levels of tannins (Remis 2002; Reynolds et al. 1998; Sommer et al. 2011). Fibrous piths and stems provide an additional source of carbohydrate energy, particularly during fruit shortages (Matsumoto-Oda and Hayashi 1999; Wrangham et al. 1991, 1998). Young leaves are probably selected for high protein content (Carlson et al. 2013; Takemoto 2003), which is generally low in fruits. High concentrations of tannins in leaves are avoided (Takemoto 2003). Overall, chimpanzees are considered to have high-quality diets (Conklin-Brittain et al. 1998).

Chimpanzees are found in habitats transformed by agriculture across their geographic range in equatorial Africa (Hockings and McLennan 2012, 2016). Crop feeding by these great apes reflects their species-typical preference for ripe sugary fruits, though a variety of nonfruit crops are also exploited (Hockings and McLennan 2012). At the borders of large uncultivated habitats, chimpanzees target particular crops in adjacent farmland, e.g., mango and sugarcane around Budongo Forest Reserve, Uganda (Tweheyo et al. 2005) and maize and banana around Kibale National Park, Uganda (Krief et al. 2014; Naughton-Treves et al. 1998). In some areas, chimpanzees survive in mosaic habitats within agroecosystems (Bessa et al. 2015; McLennan 2008) where crops can become integral to their feeding ecology (Bossou, Guinea: Hockings et al. 2009; Bulindi, Uganda: McLennan 2013).

Assimilation of cultivated foods into chimpanzee diets is a dynamic process (Takahata et al. 1986), and intriguing differences exist among populations regarding which crops are eaten and which are ignored, even where local crop assemblages are similar (McLennan and Hockings 2014). The extent to which nutritional factors drive chimpanzee foraging decisions in cultivated habitats, including which crops they exploit, remains unknown.

We here examined nutritional composition in a broad selection of wild and cultivated foods consumed by a population of wild East African chimpanzees (Pan troglodytes schweinfurthii) inhabiting a farm–forest mosaic habitat in Bulindi, Uganda. Our primary objective was to identify potential nutritional benefits of eating crops over wild foods for these chimpanzees. We first examined macronutrients and antifeedants in major categories of wild foods (fruits, piths, and leaves) to characterize nutritional properties of their natural diet. We then compared wild and cultivated foods eaten by these chimpanzees. A secondary aim was to determine if nutritional factors explain why they ignore certain crops exploited by one or more chimpanzee populations elsewhere. Thus, we compared nutrient and antifeedant concentrations in crops eaten and not eaten. We predicted that crops eaten would offer nutritional advantages over wild food equivalents, i.e., by being higher in digestible carbohydrates such as sugars and lower in insoluble fiber and antifeedants. We also predicted that crops fed on by the chimpanzees would likewise offer nutritional advantages over those crops that they ignored.

Methods

Study Site

Bulindi (1°28′N, 31°28′E) is situated in Hoima District, western Uganda, midway between the Budongo and Bugoma Forest Reserves: two main forest blocks with >500 chimpanzees each (Plumptre et al. 2010). These reserves are separated by ca. 50 km. The intervening landscape is densely populated by people (>150 persons per km2; Uganda Bureau of Statistics 2014) and dominated by subsistence and commercial agriculture (McLennan and Hill 2015). A genetic survey revealed that 260–320 chimpanzees from 9 or more resident “communities” inhabit small fragments of unprotected forest across this cultivated landscape (McCarthy et al. 2015). Chimpanzees in Bulindi represent one of these communities. Local farmers practice a combination of subsistence farming and cash-cropping. Staple food crops include cassava, potato, maize, and groundnuts, while major cash crops are tobacco, rice, and sugarcane (McLennan and Hill 2015). Domestic fruits including mango, jackfruit, banana, and papaya are grown around homes. Since the 1990s, forest clearance for timber and farming has been extensive throughout the landscape separating Budongo and Bugoma (McLennan and Hill 2015; Mwavu and Witkowski 2008; Twongyirwe et al. 2015). Primates including chimpanzees are not traditionally hunted for food in western Uganda, which enables them to persist in modified habitats near people. Consumption of agricultural crops by chimpanzees occurs throughout this region (McLennan 2008).

Chimpanzees in Bulindi were studied first in 2006–2008 (McLennan and Hill 2010). In 2012, M. R. McLennan resumed research on the chimpanzees. The community numbered 18–21 individuals during the present study in 2014–2015. Their home range exceeds 20 km2 but they usually used a core area of ca. 5 km2, comprising small patches of degraded riverine and swamp forest amid agricultural gardens and villages and dissected by a main road (McLennan and Asiimwe 2016) (Fig. 1). Common forest trees include Phoenix reclinata, Pseudospondias microcarpa, and members of the Moraceae including figs (McLennan and Plumptre 2012). About 80% of forest within the chimpanzees’ core area was cleared for farming between 2006 and 2014 (Lorenti 2014).
Fig. 1

Home range of chimpanzees in Bulindi (Hoima District, western Uganda) during this study (2014–2015), adapted from Google Earth™ 7.1.5, 2015. Dark green areas are fragments of riverine forest, Cyperus papyrus swamp, and wooded grassland; the surrounding matrix comprises smallholder farmland and homes. The yellow polygon shows the most commonly used portion of the home range, which is dissected by a main road (at center); the chimpanzees cross this road frequently (McLennan and Asiimwe 2016). Main trading centers with shops, schools, local government offices, and a police post are indicated by red ovals.

Although the chimpanzees’ diet is dominated numerically by wild plants, they forage frequently on cultivated foods in gardens and by homes, as well as from abandoned or naturalized sources (McLennan 2013; McLennan and Hockings 2014). Local tolerance of chimpanzees varies from person-to-person but crop loss to the apes is considered a worsening problem by many villagers (McLennan and Hill 2012). The chimpanzees have never been actively provisioned.

Plant Food Collection

We collected plant foods during January–April 2014, September–November 2014, March–June 2015, and October–December 2015. The chimpanzee diet at Bulindi has been well studied using a combination of indirect methods (fecal analysis and feeding trace evidence) and direct observation. At least 139 different plant food items from 103 identified species have been recorded eaten to date (McLennan 2013 and unpubl. data). During daily tracking we observed feeding behavior opportunistically and did not record feeding rates. We avoided observing chimpanzees feeding on crops, unless these were from abandoned or naturalized sources, though we sometimes encountered them foraging in gardens. During observations, we paid careful attention to food items selected and how these were processed. Similarly, we examined chimpanzee feeding traces carefully to determine the part consumed. We confirmed that the chimpanzees ate certain fruits by fecal analysis. Methods used to analyze chimpanzee feeding traces and fecal samples are detailed in McLennan (2013).

We collected 78 plant foods for this study including 44 wild and 34 cultivated items (Appendix Tables IIIV). Wild foods are predominantly native plants that are not usually planted or domesticated by humans; exceptions in the sample include native figs (Ficus natalensis and F. thonningii) that are sometimes planted around homes and paper mulberry (Broussonetia papyrifera), an exotic shrub introduced previously into nearby Budongo Forest. Its occurrence in Bulindi is presumably the result of dispersal by birds; thus we treated it as wild. Cultivated foods (synonymous with crops, cultivars, or cultigens) are domesticated plants selectively bred by people; several in our sample also occur as naturalized specimens in Bulindi, e.g., guava and tamarillo (see Spencer and Cross 2007 for a discussion of cultivated vs. wild plant definitions).

We collected three major categories of plant food: fruits (ripe and unripe), leaves (young and emerging), and piths (terrestrial herbaceous stems and leaf petioles or stems). Although chimpanzees usually ate fruits ripe, they consumed some fruits throughout the ripening process, including fully unripe. For eight such fruits, we collected ripe and unripe samples. Though the precise stage of maturity varied (Houle et al. 2014), unripe fruits were small compared to mature fruits, firm, and/or with green or pale skin and pulp. We considered leaf petioles and stems piths when the manner of processing by chimpanzees corresponded to that of terrestrial stem feeding rather than leaf feeding, i.e., leaves discarded and only the inner part of the petiole/stem eaten. Other minor food categories, e.g., seeds, tubers, flowers, and cambium, were represented by one or two foods only. Life forms of plants sampled included trees, shrubs, climbers and vines, herbs, and grasses.

Plants collected included both commonly and occasionally eaten items (as indicated by fecal analysis, direct observation, and feeding trace records; McLennan 2013). Thirteen items were crops grown at Bulindi that are reportedly eaten by one or more populations of wild chimpanzees elsewhere (Hockings and McLennan 2012), including several eaten by nearby chimpanzee communities in Hoima District (M. McCarthy, pers. comm.), but for which no evidence suggests Bulindi chimpanzees eat them (Appendix Table IV). An exception is tamarillo fruit, for which feeding traces were twice attributed to chimpanzees in 2007 (McLennan 2013). However, no further evidence has suggested the chimpanzees eat tamarillo, e.g., absence of seeds in feces and absence of feeding traces at numerous naturalized tamarillo shrubs in the forest. Thus, we consider it very unlikely that chimpanzees ate tamarillo in the present study. For all other crops not eaten (including fruits such as pineapple and staple food crops such as cassava and maize cob), there has been no evidence of consumption by the chimpanzees since research was initiated. Moreover, local farmers maintain chimpanzees do not eat these crops in Bulindi (McLennan and Hill 2012).

Wherever possible, we collected samples from actual plants that chimpanzees ate from, including intact items from feeding patches after chimpanzees fed or that fell to the ground incidentally while they fed, e.g., a fruiting or leafing branch, and partially eaten items such as large cultivated fruits, e.g., jackfruit, which are often not consumed in their entirety. We collected all partially eaten items in the same morning that chimpanzees ate them. Otherwise, we collected samples from conspecific plants showing a similar phenophase. We collected intact cultivated foods from local gardens with permission. For several crops, we failed to obtain a sample in the desired stage of maturity from local gardens, so we bought them at a market in Hoima town, 12 km from Bulindi, assuming they were of similar quality to ones consumed by the chimpanzees. Where possible, we collected samples from multiple plants of the same species.

We collected food samples in plastic bags and processed them on the same day to include only parts fed on by chimpanzees. For example, we removed outer layers of piths, leaving only the soft inner part. We removed fruit seeds and tough skins, but retained the soft fruit skins if these were normally ingested. Fecal analysis showed that chimpanzees sometimes chewed the soft bean-like seeds of Parkia filicoidea, suggesting they obtained nutrients from them. Occasionally, they ate immature seeds and pods of cultivated beans (Phaseolus vulgaris); thus, we retained a portion of the seed content for these two fruits. We took samples from crops not eaten by the chimpanzees from parts likely to be most palatable, e.g., soft fruit pulp, inner portion of piths.

After processing, we dried samples at 50–55°C using a Shef® food dehydrator. Once dry, we weighed samples, stored them in plastic bags with silica gel, and shipped 5–15 g dry weight per item to University of Hamburg, Germany, for biochemical analyses.

Nutritional Analyses

We analyzed samples for macronutrients and antifeedants via standard methods (for reviews of laboratory procedures see Ortmann et al. 2006; Rothman et al. 2012). We ground samples in a Retsch mill to a homogenous powder and dried to 50°C in the laboratory overnight. We estimated nutrient concentrations on a dry matter (DM) basis. We measured total nitrogen (TN) by the Kjeldahl method (Association of Official Analytical Chemists 1990) and determined crude protein (CP) as TN × 6.25. While this conversion factor should be adapted for different food categories, especially tropical fruits (Milton and Dintzis 1981), we use it here to allow for comparison with other studies. As CP does not necessarily reflect protein available for digestion (Rothman et al. 2008; Wallis et al. 2012), we also assessed soluble protein via the photometric BioRad assay after extraction of plant material with 0.1 N NaOH for 15 h at room temperature. A meta-analysis of primate leaf selection found that soluble protein had a greater effect on selection than TN (or CP), suggesting these protein measures differ in ecological relevance (Ganzhorn et al. 2017). Even so, TN and soluble protein correlated highly in our sample of foods (Pearson’s correlation: r = 0.593, N = 78, P < 0.0001). Further, TN in leaves from Uganda correlated well with available protein (Wallis et al. 2012). Therefore, we used CP as our measure of protein in the analysis, but we also report soluble protein in the appendices.

We analyzed neutral detergent fiber (NDF) and acid detergent fiber (ADF) using an ANKOM fiber analyzer (Van Soest et al. 1991). NDF represents the insoluble fiber (hemicellulose, cellulose, and lignin), with ADF representing the cellulose and lignin fractions; hemicellulose (HC) is thus determined by weight difference (NDF – ADF). We determined fat content (lipids) using ether extract and measured ash via combustion (Rothman et al. 2012). We extracted soluble carbohydrates and procyanidin (condensed) tannins with 50% methanol and determined soluble sugars as the equivalent of galactose after acid hydrolyzation of the methanol extract.

We measured concentrations of procyanidin tannins as equivalents of quebracho tannin using the buthanol method, and measured total phenolics (simple phenols and polyphenols) using the Folin–Ciocalteus reagent (Stolter et al. 2006). Tannins inhibit digestion by making some nutrients, e.g., proteins, unavailable for digestion. Simple phenols are small molecules that enter the cell and can act as poisons; these components are volatile and are likely to be lost during the drying process. We based analyses of polyphenols on water extracts. Standard chemical assays of these components represent poor proxies of their actual biological relevance, as both groups of chemicals comprise a plethora of substances with differing properties (Rothman et al. 2009). Nevertheless, we used these analyses to allow comparisons with other studies.

We calculated total nonstructural carbohydrate (TNC) content, i.e., the digestible carbohydrates, by subtraction following Conklin-Brittain et al. (2006):
$$ \%\mathrm{T}\mathrm{N}\mathrm{C}=100-\left(\%\mathrm{lipids}+\%\mathrm{C}\mathrm{P}+\%\mathrm{ash}+\%\mathrm{N}\mathrm{D}\mathrm{F}\right) $$
Following Conklin-Brittain et al. (2006), we applied standard conversions to nutritional fractions to calculate metabolizable energy (ME), assuming a high capacity of chimpanzees to ferment NDF, using the fiber digestion coefficient (0.543) provided by Milton and Demment (1988):
$$ \mathrm{ME}\left(\mathrm{kcal}/100\ \mathrm{g}\ \mathrm{D}\mathrm{M}\right)=4\times \%\mathrm{T}\mathrm{N}\mathrm{C}+4\times \%\mathrm{C}\mathrm{P}+9\times \%\mathrm{lipids}+1.6\times \%\mathrm{N}\mathrm{D}\mathrm{F} $$

With the exception of ME (expressed as kcal/100 g DM), we present all values as % DM.

Statistical Analysis

We examined differences between food categories in CP, lipids, soluble sugars, TNC, fiber (NDF and ADF), polyphenols and tannins, and ME. Because of unequal samples sizes and nonnormality of some distributions, we used nonparametric statistics. We compared nutritional attributes of major wild food categories (ripe fruits, piths, young leaves) using Kruskal–Wallis ANOVAs followed by Dunn–Bonferroni pairwise comparisons. We compared ripe and unripe samples from fruits that chimpanzees ate in both maturity stages using Wilcoxon signed rank tests. We used Mann–Whitney tests to assess differences between 1) crops eaten and wild food equivalents and 2) cultivated fruits eaten and not eaten; reported z-scores inform about the group with the lowest distribution. We compared wild and cultivated foods for fruit and pith only because the chimpanzees ate leaves from one crop only (yam leaves; not collected for this study). We used one-sample Wilcoxon signed rank tests to assess differences between individual nonfruit crops that were not eaten at Bulindi (but eaten elsewhere) and medians of wild food equivalents.

To control for multiple testing we applied a Holm–Bonferroni sequential adjustment to P-values in all groups of tests. This procedure is considered more powerful than the conventional Bonferroni approach, while still controlling the family-wise type I error (Abdi 2010). Nevertheless, we also report unadjusted P-values in some tests in which the adjustment was likely too conservative given small sample sizes, but these should be interpreted with caution. We performed statistical analyses using SPSS version 23 (SPSS Inc., Chicago, IL, USA) and set statistical significance at P < 0.05; all tests were two tailed.

Ethical Note

This research involving wild chimpanzees was noninvasive and adhered strictly to the legal requirements of Uganda and to ethics guidelines detailed by the Association for the Study of Animal Behaviour (UK) and the American Society of Primatologists Principles for the Ethical Treatment of Nonhuman Primates. The study was approved by the Uganda National Council for Science and Technology, the President’s Office, and the Uganda Wildlife Authority.

Results

Wild Foods Compared

Wild food categories (ripe fruits, piths, and young leaves) differed broadly in nutritional content (Fig. 2; Appendix Table II). Kruskal–Wallis tests indicated differences among categories in concentrations of CP (H = 21.25, P < 0.001), lipids (H = 8.30, P = 0.047), soluble sugars (H = 21.73, P < 0.001), total nonstructural carbohydrates (TNC) (H = 21.63, P < 0.001), fiber (NDF: H = 18.43, P < 0.001; ADF: H = 16.01, P = 0.001), polyphenols (H = 8.17, P = 0.047), and in metabolizable energy (ME) (H = 16.64, P = 0.001; df = 2 in all tests; Holm–Bonferroni adjustment applied). Pairwise comparisons showed that young leaves had significantly higher protein and lipid concentrations than both ripe fruits and piths (Fig. 2). Ripe fruits were significantly higher in soluble sugars than young leaves and tended to have higher sugar concentrations than piths, though this difference was nonsignificant after adjusting for multiple comparisons. The TNC content of fruits was higher than in both leaves and piths. Piths contained highest levels of fiber, with significantly greater NDF content than fruits and greater ADF content than both fruits and leaves. Young leaves generally had higher NDF concentrations than ripe fruits, though not significantly so after adjustment. ME was highest in ripe fruit and lowest in piths. Regarding antifeedants, leaves had significantly higher polyphenol concentrations than both fruits and piths. Tannins tended also to be highest in young leaves, although the overall Kruskal–Wallis test was nonsignificant (H = 5.13, P = 0.077 with adjustment).
Fig. 2

Chemical properties in three major categories of wild food eaten by chimpanzees in Bulindi in this study (2014–2015): ripe fruits (F; N = 21), piths (P; N = 7), and young leaves (L; N = 10). Horizontal lines inside rectangles are medians (% DM except ME, expressed as kcal/100 g); rectangles span first to third quartiles; whiskers show maximum and minimum values; open circles are outliers. Comparisons include macronutrients (crude protein, lipids, soluble sugars, total nonstructural carbohydrates [TNC]), fiber fractions (NDF, ADF), antifeedants (tannins, polyphenols), and metabolizable energy (ME). Solid horizontal lines with asterisks indicate results of post hoc Dunn–Bonferroni pairwise comparisons: *P < 0.05, **P < 0.01, ***P < 0.001; dashed horizontal lines indicate pairs that differed (P < 0.05) only before the Dunn–Bonferroni adjustment; (ns) = overall Kruskal–Wallis test nonsignificant.

Wild and Cultivated Foods Compared

Fruits Chemical composition of ripe fruits eaten by the chimpanzees differed markedly between wild and cultivated items (Fig. 3; Appendix Tables II and III). Ripe wild fruits had significantly higher concentrations of CP (z = –2.599, P = 0.047) and lipids (z = –2.747, P = 0.042), whereas ripe cultivated fruits were higher in sugar (z = –2.726, P = 0.042) and TNC (z = –3.381, P = 0.006; Holm–Bonferroni adjustment applied). Other differences were marginally nonsignificant after adjustment: ME was generally higher in cultivated fruits (z = –2.493, P = 0.051), while wild fruits showed a tendency to be higher in insoluble fiber (NDF: z = –2.282, P = 0.054; ADF: z = –2.324, P = 0.054) and polyphenols (z = –2.368, P = 0.054) (Fig. 3). While tannins were found in 10 of 21 (48%) wild fruits (range: 0.13–0.55% DM), they were found in only 2 of 10 (20%) ripe cultivated fruits eaten by the chimpanzees (0.32% DM in both cocoa and guava).
Fig. 3

Chemical properties in ripe wild fruits (W; N = 21) and ripe cultivated fruits (C; N = 10) eaten by chimpanzees in Bulindi in this study (2014–2015). For details see Fig. 2. Tannins were not detected in many fruits (not shown). Solid horizontal lines with asterisks indicate results of Mann–Whitney tests with Holm–Bonferroni adjustment: *P < 0.05, **P < 0.01; dashed horizontal lines indicate pairs that differed (P < 0.05) only before adjustment.

All eight fruits analyzed in both ripe and unripe stages (six crop fruits and two wild fruits; see Appendix Tables II and III) had higher concentrations of CP and NDF when unripe compared to when they were ripe. Conversely, ripe samples all had higher TNC content. Differences were significant before adjusting for multiple tests only (P = 0.008 in each case; Table I). As predicted, sugar concentrations were higher when fruits were ripe, with one exception: sugar content in cocoa was marginally higher in the unripe sample. ADF content was higher in unripe samples except for plantain banana, which had marginally more ADF in the ripe sample. Concentrations of lipids and antifeedants were similar in unripe and ripe stages of the fruits tested.
Table I

Chemical properties of ripe and unripe fruits of eight species (six crops and two wild species) eaten by chimpanzees at Bulindi in both stages of maturity during this study (2014–2015)

  

CP

Lipid

NDF

ADF

Sugar

TNC

CT

PP

ME

Ripe

Mdn

3.78

0.76

8.20

4.61

59.57

83.59

0.00

0.51

372.92

 

Quartiles

2.77–4.85

0.64–0.84

5.71–15.58

3.13–7.44

48.91–70.63

76.55–87.01

0.00–0.32

0.16–1.50

353.36–378.96

Unripe

Mdn

5.35

0.80

19.78

9.36

22.39

60.35

0.39

0.51

333.85

 

Quartiles

3.72–9.28

0.34–2.31

12.69–40.22

4.58–17.24

16.98–49.95

50.77–77.13

0.00–0.91

0.24–1.95

293.23–364.45

 

P

**

ns

**

*

*

**

ns

ns

*

Medians (in bold) and quartiles are shown for ripe and unripe fruits. Values are expressed as % DM except for metabolizable energy (ME), expressed as kcal/100 g. CP = crude protein; NDF = neutral detergent fiber; ADF = acid detergent fiber; Sugar = soluble sugars; TNC = total nonstructural carbohydrates; CT = condensed tannins; PP = polyphenols. Ripe and unripe fruits were compared with Wilcoxon signed rank tests. Unadjusted P-values are shown: *P < 0.05, **P < 0.01 (adjusted P-values are > 0.05); ns indicates that the unadjusted P-value was nonsignificant.

Because few wild unripe fruits were analyzed, we could not compare unripe fruits from wild and cultivated sources. However, no significant differences were apparent between wild ripe fruits and cultivated unripe fruits eaten by the chimpanzees (Electronic Supplementary Material [ESM] Fig. S1).

Piths Wild and cultivated piths eaten also varied in chemical composition (Appendix Tables II and III). Sugar and TNC concentrations, and ME, were generally higher in cultivated compared to wild piths, while ADF and polyphenol concentrations were generally lower (Fig. 4). Cultivated piths were all quite low in protein whereas some wild piths, i.e., Aframomum sp. and Marantochloa leucantha, had relatively high CP concentrations. Differences were significant only for sugars (z = –2.268, P = 0.024) and polyphenols (z = –2.462, P = 0.009), and only before controlling for multiple tests (adjusted P-values = 0.17 and 0.07, respectively). Tannins were not found in any cultivated pith analyzed.
Fig. 4

Chemical properties of wild (W; N = 7) and cultivated (C; N = 4) pith foods eaten by chimpanzees in Bulindi in this study (2014–2015). For details see Fig. 2. Tannins (not shown) were not detected in any cultivated pith analyzed, but were present in three of seven wild piths eaten. Dashed horizontal lines indicate pairs that differed (P < 0.05) before applying a Holm–Bonferroni adjustment.

Crops Eaten and Not Eaten Compared

Some differences were apparent between the 10 ripe cultivated fruits eaten and 6 that were not eaten (Appendix Tables III and IV). Those eaten were lower in CP (z = –2.768, P = 0.039; Fig. 5) but higher in TNC (z = –2.820, P = 0.038; Holm–Bonferroni adjustment applied). Crop fruits eaten also tended to have lower lipid and NDF concentrations than those not eaten, but these differences were nonsignificant after controlling for multiple tests (P = 0.10 and 0.11, respectively). No differences were apparent in other nutrients tested, including sugars. Small concentrations of tannins were found in only 3 of the 16 ripe cultivated fruits: cocoa and guava (eaten) and soursop (not eaten).
Fig. 5

Chemical properties of ripe cultivated fruits eaten (N = 10) and not eaten (N = 6) by the chimpanzees in this study (2014–2015). For details see Fig. 2. Tannins were not detected in most cultivated fruits (not shown). The ^ symbol indicates the lipid content of avocado fruit was exceptionally high: 40.3% DM (not shown to scale for readability); all other crop fruits had lipid concentrations 0.3–2.4% DM. Solid horizontal lines with asterisks indicate results of Mann–Whitney tests with Holm–Bonferroni adjustment: *P < 0.05; dashed horizontal lines indicate pairs that differed (P < 0.05) only before adjustment.

Papaya leaf, which the chimpanzees did not eat, was higher in CP (29.9% DM) than all 10 wild young leaf species that they did eat (Mdn = 22.7%; one-sample Wilcoxon signed rank test: P = 0.040 with Holm–Bonferroni adjustment). In fact, papaya leaf was highest in protein of all 78 foods analyzed (appendices). Papaya leaves were also low in polyphenols (0.78%) compared to most wild leaf foods (Mdn = 1.48%), though this difference was nonsignificant after adjustment (unadjusted P = 0.028; adjusted P = 0.196). While tannins were not found in papaya leaf, they were present in 7 of 10 wild young leaf foods. Papaya pith, also not eaten, was lower in fiber (NDF = 18.35%, ADF = 13.42%) than all 7 wild piths analyzed (Mdn = 37.64% and 23.37%, respectively), while its ME content was highest (305.14 kcal/100 g vs. 264.70 kcal/100 g [Mdn] for wild piths). A second cultivated pith not eaten at Bulindi (rice) was lower in polyphenols (0.15%) than all wild piths analyzed (Mdn = 0.61%). Only unadjusted P-values were significant (P = 0.018 in each case). Notably, both rice and papaya pith had considerably higher levels of CP (13.4% and 14.2%, respectively) than the four cultivated piths that the chimpanzees did eat (1.8–8.4%; Appendix Tables III and IV). Conversely, sugar concentrations in rice and papaya pith were lower and more similar to those in wild pith foods. The fiber and polyphenol content was overall similar in cultivated piths eaten and not eaten. None of the cultivated piths contained tannins.

Four additional crops analyzed—not eaten by the chimpanzees—are staple foods for local people: cassava and sweet potato (tubers), maize cob (caryopsis), and ground nuts (seed crop). There were no wild food equivalents for these in our sample. These crops were generally low in soluble sugars (Appendix Table IV). However, cassava and maize cob in particular are high in starch (United States Department of Agriculture 2016), which we did not assay. Fiber concentrations in cassava, maize cob, and ground nuts were within the range of other nonfruit items eaten by the chimpanzees. However, sweet potato was high in NDF (58.9%)—almost all hemicellulose. The fiber content of cassava and maize similarly comprised mostly hemicellulose. Ground nuts were rich in protein and contained an exceptionally high lipid concentration. All staple food crops were low in antifeedants.

Discussion

Our results support the common assertion that crops offer certain nutritional advantages over wild plants for primates in human-modified environments. Chimpanzees within the forest–agricultural mosaic in Bulindi supplement a “natural” diet with various cultivated foods that compared to wild food equivalents, and in accord with our prediction, had higher levels of easily digestible carbohydrates (mainly sugars) coupled with reduced amounts of insoluble fiber and antifeedants. Conversely, however, crops eaten by the chimpanzees were not a good source of protein or lipids relative to some wild foods, which may be true of cultivars generally (Milton 1999). In addition, compared to crops, wild plants may contain higher concentrations of essential micronutrients (vitamins and minerals) that we did not assay here (Milton 1999; cf. Rode et al. 2006). Whether crop feeding primates balance their nutrient intake, e.g., with protein or lipid-rich wild foods, is largely unknown. However, Johnson et al. (2013) demonstrated nutrient balancing in a female Papio ursinus, which included exotic plants and other “human-derived” foods in its diet. Because we did not measure feeding time or food intake by the chimpanzees, we could not estimate nutrient intake. Thus, further research is needed to determine how the chimpanzees prioritize and regulate nutrient intake through their choice of wild and cultivated foods to understand better the role of crops in meeting their nutritional requirements (Felton et al. 2009; Lambert and Rothman 2015).

Besides chemical properties, other characteristics of crops suggest they offer enhanced foraging efficiency over many wild foods. When grown in fields, orchards, and plantations, crops present a predictable, spatially abundant and concentrated food source, requiring little search time. Crops also frequently come in large “packages.” Jackfruits, for example, are the largest tree-borne fruit, weighing up to 35 kg (Prakash et al. 2009); a single large jackfruit easily satisfies an adult chimpanzee (McLennan, pers. obs.) (Fig. 6). In addition, crop fruits usually have low seed-to-pulp ratios relative to wild fruits (Milton 1999). Overall, crops are easier to find, process, and digest than many wild foods, providing more energy for less effort (Forthman-Quick and Demment 1988; Strum 2010).
Fig. 6

Some crops in the diet of chimpanzees in Bulindi, 2014–2015. (a) Adult male eating ripe jackfruit. (b) Subadult female eating unripe jackfruit. (c) Adult males from a nearby community eating pith of commercially grown sugarcane. (d) Damage to banana plants after chimpanzees ate the inner pith. (e) Naturalized guava, a common food for chimpanzees in Bulindi. (f) Partially eaten unripe cocoa pods. (g) Partially eaten unripe mangos. (h) Subadult male eating ripe mango. (i) Partially eaten semiripe papaya fruit. (j) Adult male in a cassava field; cassava is a staple food crop for humans but chimpanzees in Bulindi do not feed on any part of the plant. (k) Adult male by a field of ripening maize, also a staple food crop. Though chimpanzees in Bulindi ignore the cob, they occasionally eat pith from young maize plants (l). Photographs by Matthew McLennan except (h) and (k) by Georgia Lorenti.

Our analysis of the chimpanzees’ wild plant diet at Bulindi corresponds with previous chemical analyses of primate plant foods (Lambert and Rothman 2015): ripe fruits provided energy from easily digestible carbohydrates, i.e., sugars; piths were an alternative source of carbohydrate energy, particularly from fiber; and young leaves provided protein, which was low in fruits. Plants eaten by wild primates generally contain low amounts of lipids (Lambert and Rothman 2015; Rothman et al. 2012), as was true of wild plants analyzed here. While previous studies found that ripe fruits provided the majority of lipids in African ape diets (Conklin-Brittain et al. 1998; Reiner et al. 2014), lipids were highest in young leaves in our sample. However, this high “lipid” content likely includes nonnutritive components such as wax and cutin that are also extracted by ether (Palmquist and Jenkins 2003). Nevertheless, individual plants within major food categories—both wild and cultivated—varied considerably in chemical properties (Appendix Tables II and III).

Though unripe fruit contained less digestible carbohydrates and more fiber compared to when fully ripe, it offered a supplementary source of protein and energy. We found no differences in antifeedant content between unripe and ripe samples. However, most fruits sampled in both maturity stages were crops that, relative to wild foods, had small concentrations of polyphenols generally and rarely contained tannins (appendices). Though our sample of unripe fruits was small, the absence of strong differences between unripe cultivated fruits and ripe wild fruits suggests agricultural fruits are relatively nutritious throughout the ripening process. Indeed, chimpanzees often ate unripe fruits of cocoa, mango, jackfruit, and guava when available (McLennan, unpubl. data) (Fig. 6). Again, however, nutrient concentrations in unripe fruits varied considerably. For example, unripe fruit of cocoa, mango, and papaya had sugar levels comparable to those of ripe fruits of many wild species. Conversely, unripe plantain banana contained very little soluble sugar, but may have instead provided energy from hemicellulose (Appendix Table III).

Why Did Chimpanzees Ignore Certain Crops?

Contrary to prediction, we found little evidence that crops ignored by the chimpanzees were less nutritious than those that they did eat. Compared to cultivated fruits eaten, ignored fruits (avocado, pineapple, pumpkin, soursop, tamarillo, and tomato) tended to be lower in nonstructural carbohydrates and more fibrous, which might have influenced whether chimpanzees chose to eat them or not. Conversely, the ignored fruits were a better source of protein and lipids, although chimpanzees probably select ripe fruits primarily for their digestibility and high sugar content. Still, pineapple had among the highest sugar content of all fruits analyzed and should have been highly attractive to chimpanzees. Moreover, all ignored fruits are highly palatable to humans, with the exception of pumpkin, which—although edible raw—is considered too fibrous to eat uncooked by local people, although other primates in Bulindi readily eat it, e.g., Chlorocebus tantalus.

Two cultivated piths not eaten by the chimpanzees (rice stem and papaya leaf petiole) offered a good source of protein with low concentrations of fiber and antifeedants. Still, the greater sugar content of cultivated piths that were eaten (especially sugarcane and yam pith, which had sugar concentrations comparable to crop fruits; Appendix Table III), suggests chimpanzees at Bulindi selected cultivated piths mainly for their sweet taste (or carbohydrate energy), not protein. Young leaves of papaya had the highest amount of crude protein of all foods analyzed. But no evidence suggested the chimpanzees exploit this protein-rich resource (as chimpanzees do at Bossou, for example; Hockings and McLennan 2012), although they often ate papaya fruit.

Nonnutritional factors probably also influence crop selection by primates. In this study, we did not compare availability or abundance of different crops, which might influence whether chimpanzees eat them or not (McLennan and Hockings 2014). With regards to fruits, soursop trees were rare at Bulindi and chimpanzees probably had limited opportunities to encounter the sweet fruits. But other crop fruits not eaten such as pineapple, pumpkin, tamarillo, and tomato were more common than several that were eaten, e.g., lemon, orange, and passion fruit. Other nonfruit crops that were ignored—particularly staple foods for local people such as cassava, maize, sweet potato, and rice—were highly abundant and chimpanzees encountered these foods daily when seasonally available. Thus, availability cannot explain why they did not eat them. In particular, maize cob is among the crops most commonly targeted by chimpanzees across Africa (Hockings and McLennan 2012). Crops that are comparable to wild foods in shape, color, and/or odor, and requiring similar processing, are most likely to be recognized as edible by wildlife (McLennan and Hockings 2014). Chimpanzees probably recognize many fruit crops as palatable from ripeness cues, but some fruits ignored at Bulindi, e.g., avocado and pineapple, are harvested by humans before fully ripe and thus lack a strongly sweet odor, or are encased within a tough exocarp such as pumpkin. However, chimpanzees readily consume cocoa pods, which are similarly tough and not strongly scented. In Bulindi, chimpanzees seem not to have parallels in their natural diet for crops such as cassava tuber, sweet potato, and groundnuts (which are embedded) and maize cob (which is concealed). Such characteristics may help explain why they do not currently exploit them.

A previous study showed that chimpanzees at Bossou, where apes have exploited crops for generations, ate a greater variety of cultivated foods (including staple food crops such as cassava, rice, and maize cob) compared to Bulindi, where major habitat encroachment is more recent (McLennan and Hockings 2014). Fast-changing mosaic landscapes may generate dynamic feeding patterns in wild animals, involving complex interactions between local anthropogenic and environmental factors, e.g., farming practices and the relative availability and nutritional quality of wild and cultivated foods (McLennan and Hockings 2014). Thus, chimpanzees in Bulindi may yet “discover” that certain crops not currently exploited are good to eat in time, as illustrated by Takahata et al. (1986), who described the gradual assimilation of mango, guava, and lemon into the diet of wild chimpanzees at Mahale, Tanzania.

Sustainability of Primate Crop Feeding

Ongoing human settlement and cultivation, especially in the tropics, means that primates should adjust their behavior to survive in modified landscapes, or else go locally extinct (Anderson et al. 2007; Estrada et al. 2012; Nowak and Lee 2013). Supplementing a natural diet with energy-rich crops is one such adjustment, but crop foraging inevitably brings primates into competition with humans (Paterson and Wallis 2005). The relative costs and benefits of eating crops will differ according to species and habitat and, perhaps most importantly, human cultural attitudes and socioeconomic conditions that define tolerance of wildlife, but are subject to change (Hill and Webber 2010; McLennan and Hill 2012; Naughton-Treves and Treves 2005; Riley 2010). Like many primates, chimpanzees show a high level of behavioral and dietary flexibility that enables them to survive in cultivated habitats, providing they are not hunted or persecuted (Hockings et al. 2015; Hockings and McLennan 2016). Despite the tolerance sometimes afforded apes by human cultural beliefs, persistent crop losses and associated problems, i.e., aggression toward people (McLennan and Hockings 2016), can instigate retributive killings and use of lethal control methods (Hyeroba et al. 2011; McLennan et al. 2012; Meijaard et al. 2011). Chimpanzees have slow life histories, and even occasional trappings and killings cause population declines (Hockings and McLennan 2016). Whether agricultural and other matrix habitats can support populations of threatened but flexible primates such as chimpanzees in the long term is uncertain. Ultimately, it hinges on the willingness and capacity of local people to share their landscape and resources with them.

Notes

Acknowledgements

We are grateful to the President’s Office, the Uganda National Council for Science and Technology, and the Uganda Wildlife Authority for permission to study the chimpanzees of Bulindi. Matthew McLennan’s fieldwork was supported by a fellowship from the Leverhulme Trust. We are particularly grateful to Tom Sabiiti for assistance in the field. For help with the chemical analyses we thank Irene Tomaschewski. Mary Namaganda and Olivia Maganyi at Makerere University Herbarium, Uganda, identified the taxonomy of several plants analyzed for this study. We thank Kimberley Hockings, Noemi Spagnoletti, Giuseppe Donati, Joanna Setchell, and the reviewers for helpful comments on the draft manuscript.

Compliance with Ethical Standards

Conflict of Interest

The authors declare no conflicts of interest or competing financial interest.

Supplementary material

10764_2016_9940_MOESM1_ESM.docx (211 kb)
Fig. S1(DOCX 211 kb)

References

  1. Abdi, H. (2010). Holm’s sequential Bonferroni procedure. In N. Salkind (Ed.), Encyclopedia of research design (pp. 573–577). Thousand Oaks: SAGE.Google Scholar
  2. Altmann, J., & Muruthi, P. (1988). Differences in daily life between semiprovisioned and wild‐feeding baboons. American Journal of Primatology, 15, 213–221.CrossRefGoogle Scholar
  3. Anderson, J., Rowcliffe, J. M., & Cowlishaw, G. (2007). Does the matrix matter? A forest primate in a complex agricultural landscape. Biological Conservation, 135, 212–222.CrossRefGoogle Scholar
  4. Association of Official Analytical Chemists. (1990). Official methods of analysis. Arlington: Association of Official Analytical Chemists.Google Scholar
  5. Bessa, J., Sousa, C., & Hockings, K. J. (2015). Feeding ecology of chimpanzees (Pan troglodytes verus) inhabiting a forest‐mangrove‐savanna‐agricultural matrix at Caiquene‐Cadique, Cantanhez National Park, Guinea‐Bissau. American Journal of Primatology, 77, 651–665.CrossRefPubMedGoogle Scholar
  6. Bicca-Marques, J. C., & Calegaro-Marques, C. (1994). Exotic plant species can serve as staple food sources for wild howler populations. Folia Primatologica, 63, 209–211.CrossRefGoogle Scholar
  7. Brennan, E. J., Else, J. G., & Altmann, J. (1985). Ecology and behaviour of a pest primate: Vervet monkeys in a tourist‐lodge habitat. African Journal of Ecology, 23, 35–44.CrossRefGoogle Scholar
  8. Carlson, B. A., Rothman, J. M., & Mitani, J. C. (2013). Diurnal variation in nutrients and chimpanzee foraging behavior. American Journal of Primatology, 75, 342–349.CrossRefPubMedGoogle Scholar
  9. Chapman, C. A., Speirs, M. L., Gillespie, T. R., Holland, T., & Austad, K. M. (2006). Life on the edge: Gastrointestinal parasites from the forest edge and interior primate groups. American Journal of Primatology, 68, 397–409.CrossRefPubMedGoogle Scholar
  10. Conklin-Brittain, N. L., Wrangham, R. W., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. Macronutrients. International Journal of Primatology, 19, 971–998.CrossRefGoogle Scholar
  11. Conklin-Brittain, N. L., Knott, C. D., & Wrangham, R. W. (2006). Energy intake by wild chimpanzees and orangutans: Methodological considerations and a preliminary comparison. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 445–472). Cambridge: Cambridge University Press.Google Scholar
  12. Conover, M. R. (2002). Resolving human–wildlife conflicts: The science of wildlife damage management. Boca Raton: Lewis Publishers.Google Scholar
  13. Dostaler, S., Ouellet, J. P., Therrien, J. F., & Côté, S. D. (2011). Are feeding preferences of white‐tailed deer related to plant constituents? Journal of Wildlife Management, 75, 913–918.CrossRefGoogle Scholar
  14. Eley, R. M., Strum, S .C., Muchemi, G., & Reid, G. D .F. (1989). Nutrition, body condition, activity patterns, and parasitism of free‐ranging troops of olive baboons (Papio anubis) in Kenya. American Journal of Primatology, 18, 209–219.Google Scholar
  15. Estrada, A., Raboy, B. E., & Oliveira, L. C. (2012). Agroecosystems and primate conservation in the tropics: A review. American Journal of Primatology, 74, 696–711.CrossRefPubMedGoogle Scholar
  16. Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009). Nutritional goals of wild primates. Functional Ecology, 23, 70–78.CrossRefGoogle Scholar
  17. Forthman-Quick, D. L., & Demment, M. W. (1988). Dynamics of exploitation: Differential energetic adaptations of two troops of baboons to recent human contact. In J. E. Fa & C. H. Southwick (Eds.), Ecology and behavior of food-enhanced primate groups (pp. 25–51). New York: Alan R. Liss.Google Scholar
  18. Ganzhorn, J. U., Arrigo‐Nelson, S. J., Carrai, V., Chalise, M. K., Donati, G., et al. (2017). The importance of protein in leaf selection of folivorous primates. American Journal of Primatology. doi:10.1002/ajp.22550.Google Scholar
  19. Ghiglieri, M. P. (1984). The chimpanzees of Kibale Forest: A field study of ecology and social structure. New York: Columbia University Press.Google Scholar
  20. Gibbs, H. K., Ruesch, A. S., Achard, F., Clayton, M. K., Holmgren, P., et al. (2010). Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proceedings of the National Academy of Sciences of the USA, 107, 16732–16737.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hill, C. M. (1997). Crop-raiding by wild vertebrates: The farmer’s perspective in an agricultural community in western Uganda. International Journal of Pest Management, 43, 77–84.CrossRefGoogle Scholar
  22. Hill, C. M. (2000). Conflict of interest between people and baboons: Crop raiding in Uganda. International Journal of Primatology, 21, 299–315.CrossRefGoogle Scholar
  23. Hill, C. M., & Webber, A. D. (2010). Perceptions of nonhuman primates in human–wildlife conflict scenarios. American Journal of Primatology, 72, 919–924.CrossRefPubMedGoogle Scholar
  24. Hockings, K. J., & McLennan, M. R. (2012). From forest to farm: Systematic review of cultivar feeding by chimpanzees: Management implications for wildlife in anthropogenic landscapes. PLoS ONE, 7, e33391.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hockings, K. J., & McLennan, M. R. (2016). Problematic primate behaviour in agricultural landscapes: Chimpanzees as ‘pests’ and ‘predators.’ In M. Waller (Ed.), Ethnoprimatology: Primate conservation in the 21st century (pp. 137–156). Developments in Primatology: Progress and Prospects. Cham, Switzerland: Springer.Google Scholar
  26. Hockings, K. J., Anderson, J. R., & Matsuzawa, T. (2009). Use of wild and cultivated foods by chimpanzees at Bossou, Republic of Guinea: Feeding dynamics in a human-influenced environment. American Journal of Primatology, 71, 636–646.CrossRefPubMedGoogle Scholar
  27. Hockings, K. J., McLennan, M. R., Carvalho, S., Ancrenaz, M., Bobe, R., et al. (2015). Apes in the Anthropocene: Flexibility and survival. Trends in Ecology & Evolution, 30, 215–222.CrossRefGoogle Scholar
  28. Hohmann, G., Potts, K., N’Guessan, A., Fowler, A., Mundry, R., et al. (2010). Plant foods consumed by Pan: Exploring the variation of nutritional ecology across Africa. American Journal of Physical Anthropology, 141, 476–485.PubMedGoogle Scholar
  29. Houle, A., Conklin‐Brittain, N. L., & Wrangham, R. W. (2014). Vertical stratification of the nutritional value of fruit: Macronutrients and condensed tannins. American Journal of Primatology, 76, 1207–1232.CrossRefPubMedGoogle Scholar
  30. Hyeroba, D., Apell, P., & Otali, E. (2011). Managing a speared alpha male chimpanzee (Pan troglodytes) in Kibale National Park, Uganda. Veterinary Record, 169, 658.CrossRefPubMedGoogle Scholar
  31. Johnson, C. A., Raubenheimer, D., Rothman, J. M., Clarke, D., & Swedell, L. (2013). 30 Days in the life: Daily nutrient balancing in a wild chacma baboon. PLoS ONE, 8, e70383.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kemnitz, J. W., Sapolsky, R. M., Altmann, J., Muruthi, P., Mott, G. E., & Stefanick, M. L. (2002). Effects of food availability on serum insulin and lipid concentrations in free‐ranging baboons. American Journal of Primatology, 57, 13–19.CrossRefPubMedGoogle Scholar
  33. Krief, S., Cibot, M., Bortolamiol, S., Seguya, A., Krief, J. M., & Masi, S. (2014). Wild chimpanzees on the edge: Nocturnal activities in croplands. PLoS ONE, 9, e109925.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lambert, J. E., & Rothman, J. M. (2015). Fallback foods, optimal diets, and nutritional targets: Primate responses to varying food availability and quality. Annual Review of Anthropology, 44, 493–512.CrossRefGoogle Scholar
  35. Laurance, W. F., Sayer, J., & Cassman, K. G. (2014). Agricultural expansion and its impacts on tropical nature. Trends in Ecology & Evolution, 29, 107–116.CrossRefGoogle Scholar
  36. Lodge, E., Ross, C., Ortmann, S., & MacLarnon, A. M. (2013). Influence of diet and stress on reproductive hormones in Nigerian olive baboons. General and Comparative Endocrinology, 191, 146–154.CrossRefPubMedGoogle Scholar
  37. Lorenti, G. (2014). Assessing fragmentation characteristics at Bulindi, western Uganda: Implications for primate conservation in a fragmented landscape. MSc dissertation, Oxford Brookes University.Google Scholar
  38. Mackenzie, C. A., & Ahabyona, P. (2012). Elephants in the garden: Financial and social costs of crop raiding. Ecological Economics, 75, 72–82.CrossRefGoogle Scholar
  39. Matsumoto-Oda, A., & Hayashi, Y. (1999). Nutritional aspects of fruit choice by chimpanzees. Folia Primatologica, 70, 154–162.CrossRefGoogle Scholar
  40. McCarthy, M. S., Lester, J. D., Howe, E. J., Arandjelovic, M., Stanford, C. B., & Vigilant, L. (2015). Genetic censusing identifies an unexpectedly sizeable population of an endangered large mammal in a fragmented forest landscape. BMC Ecology, 15, 21.CrossRefPubMedPubMedCentralGoogle Scholar
  41. McKinney, T. (2011). The effects of provisioning and crop‐raiding on the diet and foraging activities of human‐commensal white‐faced capuchins (Cebus capucinus). American Journal of Primatology, 73, 439–448.CrossRefPubMedGoogle Scholar
  42. McLennan, M. R. (2008). Beleaguered chimpanzees in the agricultural district of Hoima, western Uganda. Primate Conservation, 23, 45–54.CrossRefGoogle Scholar
  43. McLennan, M. R. (2013). Diet and feeding ecology of chimpanzees (Pan troglodytes) in Bulindi, Uganda: Foraging strategies at the forest–farm interface. International Journal of Primatology, 34, 585–614.CrossRefGoogle Scholar
  44. McLennan, M. R., & Asiimwe, C. (2016). Cars kill chimpanzees: Case report of a wild chimpanzee killed on a road at Bulindi, Uganda. Primates, 57, 377–388.CrossRefPubMedGoogle Scholar
  45. McLennan, M. R., & Hill, C. M. (2010). Chimpanzee responses to researchers in a disturbed forest–farm mosaic at Bulindi, western Uganda. American Journal of Primatology, 72, 907–918.CrossRefPubMedGoogle Scholar
  46. McLennan, M. R., & Hill, C. M. (2012). Troublesome neighbours: Changing attitudes towards chimpanzees (Pan troglodytes) in a human-dominated landscape in Uganda. Journal for Nature Conservation, 20, 219–227.CrossRefGoogle Scholar
  47. McLennan, M. R., & Hill, C. M. (2015). Changing agricultural practices and human–chimpanzee interactions: Tobacco and sugarcane farming in and around Bulindi, Uganda. In Arcus Foundation (Ed.), State of the apes: Industrial agriculture and ape conservation (pp. 29–31). Cambridge: Cambridge University Press.Google Scholar
  48. McLennan, M. R., & Hockings, K. J. (2014). Wild chimpanzees show group differences in selection of agricultural crops. Scientific Reports, 4, 5956.CrossRefPubMedPubMedCentralGoogle Scholar
  49. McLennan, M. R., & Hockings, K. J. (2016). The aggressive apes? Causes and contexts of great ape attacks on humans. In F. M. Angelici (Ed.), Problematic wildlife: A cross-disciplinary approach (pp. 373–394). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  50. McLennan, M. R., & Plumptre, A. J. (2012). Protected apes, unprotected forest: Composition, structure and diversity of riverine forest fragments and their conservation value in Uganda. Tropical Conservation Science, 5, 79–103.CrossRefGoogle Scholar
  51. McLennan, M. R., Hyeroba, D., Asiimwe, C., Reynolds, V., & Wallis, J. (2012). Chimpanzees in mantraps: Lethal crop protection and conservation in Uganda. Oryx, 41, 598–603.CrossRefGoogle Scholar
  52. Meijaard, E., Buchori, D., Hadiprakarsa, Y., Utami-Atmoko, S. S., Nurcahyo, A., et al. (2011). Quantifying killing of orangutans and human–orangutan conflict in Kalimantan, Indonesia. PLoS ONE, 6, e27491.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Milton, K. (1999). Nutritional characteristics of wild primate foods: Do the diets of our closest living relatives have lessons for us? Nutrition, 15, 488–498.CrossRefPubMedGoogle Scholar
  54. Milton, K., & Demment, M. W. (1988). Digestion and passage kinetics of chimpanzees fed high and low fiber diets and comparison with human data. Journal of Nutrition, 118, 1082–1088.PubMedGoogle Scholar
  55. Milton, K., & Dintzis, F. R. (1981). Nitrogen-to-protein conversion factors for tropical plant samples. Biotropica, 13, 177–181.CrossRefGoogle Scholar
  56. Mwavu, E. N., & Witkowski, E. T. F. (2008). Land-use and cover changes (1988–2002) around Budongo Forest Reserve, NW Uganda: Implications for forest and woodland sustainability. Land Degradation and Development, 19, 606–622.CrossRefGoogle Scholar
  57. Naughton-Treves, L., & Treves, A. (2005). Socio-ecological factors shaping local support for wildlife: Crop-raiding by elephants and other wildlife in Africa. In R. Woodroffe, S. Thirgood, & A. Rabinowitz (Eds.), People and wildlife: Conflict or coexistence? (pp. 252–277). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  58. Naughton-Treves, L., Treves, A., Chapman, C., & Wrangham, R. (1998). Temporal patterns of crop-raiding by primates: Linking food availability in croplands and adjacent forest. Journal of Applied Ecology, 35, 596–606.CrossRefGoogle Scholar
  59. Nijman, V. (2012). Purple-faced langurs in human-modified environments feeding on cultivated fruits: A comment to Dela (2007, 2012). International Journal of Primatology, 33, 743–748.CrossRefGoogle Scholar
  60. Nowak, K., & Lee, P. C. (2013). “Specialist” primates can be flexible in response to habitat alteration. In L. K. Marsh & C. A. Chapman (Eds.), Primates in fragments: Complexity and resilience (pp. 199–211). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.Google Scholar
  61. Ortmann, S., Bradley, B. J., Stolter, C., & Ganzhorn, J. U. (2006). Estimating the quality and composition of wild animal diets: A critical survey of methods. In G. Hohmann, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 395–418). Cambridge: Cambridge University Press.Google Scholar
  62. Osborn, F. V. (2004). Seasonal variation of feeding patterns and food selection by crop‐raiding elephants in Zimbabwe. African Journal of Ecology, 42, 322–327.CrossRefGoogle Scholar
  63. Palmquist, D. L., & Jenkins, T. C. (2003). Challenges with fats and fatty acid methods. Journal of Animal Science, 81, 3250–3254.CrossRefPubMedGoogle Scholar
  64. Paterson, J. D., & Wallis, J. (2005). Commensalism and conflict: The human–primate interface. Norman: American Society of Primatologists.Google Scholar
  65. Plumptre, A. J., Rose, R., Nangendo, G., Williamson, E. A., Didier, K., et al. (2010). Eastern chimpanzee (Pan troglodytes schweinfurthii) status survey and conservation action plan: 2010–2020. Gland: IUCN.Google Scholar
  66. Prakash, O., Kumar, R., Mishra, A., & Gupta, R. (2009). Artocarpus heterophyllus (Jackfruit): An overview. Pharmacognosy Reviews, 3, 353–358.Google Scholar
  67. Priston, N. E., & McLennan, M. R. (2013). Managing humans, managing macaques: Human–macaque conflict in Asia and Africa. In S. Radhakrishna, M. A. Huffman, & A. Sinha (Eds.), The macaque connection: Cooperation and conflict between humans and macaques (pp. 225–250). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.Google Scholar
  68. Redpath, S. M., Young, J., Evely, A., Adams, W. M., Sutherland, W. J., et al. (2013). Understanding and managing conservation conflicts. Trends in Ecology & Evolution, 28, 100–109.CrossRefGoogle Scholar
  69. Reiner, W. B., Petzinger, C., Power, M. L., Hyeroba, D., & Rothman, J. M. (2014). Fatty acids in mountain gorilla diets: Implications for primate nutrition and health. American Journal of Primatology, 76, 281–288.CrossRefPubMedGoogle Scholar
  70. Remis, M. J. (2002). Food preferences among captive western gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes). International Journal of Primatology, 23, 231–249.CrossRefGoogle Scholar
  71. Reynolds, V., Plumptre, A. J., Greenham, J., & Harborne, J. (1998). Condensed tannins and sugars in the diet of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda. Oecologia, 115, 331–336.CrossRefPubMedGoogle Scholar
  72. Riley, E. P. (2010). The importance of human-macaque folklore for conservation in Lore Lindu National Park, Sulawesi, Indonesia. Oryx, 44, 235–240.CrossRefGoogle Scholar
  73. Riley, E. P., Tolbert, B., & Farida, W. R. (2013). Nutritional content explains the attractiveness of cacao to crop raiding Tonkean macaques. Current Zoology, 59, 160–169.CrossRefGoogle Scholar
  74. Rode, K. D., Chiyo, P. I., Chapman, C. A., & McDowell, L. R. (2006). Nutritional ecology of elephants in Kibale National Park, Uganda, and its relationship with crop-raiding behaviour. Journal of Tropical Ecology, 22, 441–449.CrossRefGoogle Scholar
  75. Rothman, J. M., Chapman, C. A., & Pell, A. N. (2008). Fiber‐bound nitrogen in gorilla diets: Implications for estimating dietary protein intake of primates. American Journal of Primatology, 70, 690–694.CrossRefPubMedGoogle Scholar
  76. Rothman, J. M., Dusinberre, K., & Pell, A. N. (2009). Condensed tannins in the diets of primates: A matter of methods? American Journal of Primatology, 71, 70–76.CrossRefPubMedGoogle Scholar
  77. Rothman, J. M., Chapman, C. A., & Van Soest, P. J. (2012). Methods in primate nutritional ecology: A user’s guide. International Journal of Primatology, 33, 542–566.CrossRefGoogle Scholar
  78. Saj, T., Sicotte, P., & Paterson, J. D. (1999). Influence of human food consumption on the time budget of vervets. International Journal of Primatology, 20, 977–994.CrossRefGoogle Scholar
  79. Seiler, N., & Robbins, M. M. (2016). Factors influencing ranging on community land and crop raiding by mountain gorillas. Animal Conservation, 17, 176–188.CrossRefGoogle Scholar
  80. Sommer, V., Bauer, J., Fowler, A., & Ortmann, S. (2011). Patriarchal chimpanzees, matriarchal bonobos: Potential ecological causes of a Pan dichotomy. In V. Sommer & C. Ross (Eds.), Primates of Gashaka (pp. 469–501). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.Google Scholar
  81. Spagnoletti, N., Cardoso, T. C. M., Fragaszy, D., & Izar, P. (2017). Coexistence between humans and capuchins (Sapajus libidinosus): Comparing observational data with farmers’ perceptions of crop losses. International Journal of Primatology. doi:10.1007/s10764-016-9926-9.
  82. Spencer, R. D., & Cross, R. G. (2007). The International Code of Botanical Nomenclature (ICBN), the International Code of Nomenclature for Cultivated Plants (ICNCP), and the cultigen. Taxon, 56, 938–940.CrossRefGoogle Scholar
  83. Stolter, C., Julkunen-Tiitto, R., & Ganzhorn, J. U. (2006). Application of near infrared reflectance spectroscopy (NIRS) to assess some properties of a sub-arctic ecosystem. Basic and Applied Ecology, 7, 167–187.CrossRefGoogle Scholar
  84. Strum, S. C. (2010). The development of primate raiding: Implications for management and conservation. International Journal of Primatology, 31, 133–156.CrossRefPubMedPubMedCentralGoogle Scholar
  85. Sugiyama, Y., & Ohsawa, H. (1982). Population dynamics of Japanese monkeys with special reference to the effect of artificial feeding. Folia Primatologica, 39, 238–263.CrossRefGoogle Scholar
  86. Takahata, Y., Hiraiwa-Hasegawa, M., Takasaki, H., & Nyundo, R. (1986). Newly acquired feeding habits among the chimpanzees of the Mahale Mountains National Park, Tanzania. Human Evolution, 1, 277–284.CrossRefGoogle Scholar
  87. Takemoto, H. (2003). Phytochemical determination for leaf food choice by wild chimpanzees in Guinea, Bossou. Journal of Chemical Ecology, 29, 2551–2573.CrossRefPubMedGoogle Scholar
  88. Tilman, D., Fargione, J., Wolff, B., D’Antonio, C., Dobson, A., et al. (2001). Forecasting agriculturally driven global environmental change. Science, 292, 281–284.CrossRefPubMedGoogle Scholar
  89. Tweheyo, M., Hill, C. M., & Obua, J. (2005). Patterns of crop raiding by primates around the Budongo Forest Reserve, Uganda. Wildlife Biology, 11, 237–247.CrossRefGoogle Scholar
  90. Twongyirwe, R., Bithell, M., Richards, K. S., & Rees, W. G. (2015). Three decades of forest cover change in Uganda’s northern Albertine Rift landscape. Land Use Policy, 49, 236–251.CrossRefGoogle Scholar
  91. Uganda Bureau of Statistics. (2014). National population and housing census 2014: Provisional results. Kampala: Uganda Bureau of Statistics.Google Scholar
  92. United States Department of Agriculture. (2016). National Nutrient Database for Standard Reference, Release 28 (slightly revised May 2016). United States Department of Agriculture, Agricultural Research Service, Nutrient Data Laboratory. https://ndb.nal.usda.gov/. Accessed 1 July 2016.
  93. Van Soest, P. V., Robertson, J. B., & Lewis, B. A. (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74, 3583–3597.CrossRefPubMedGoogle Scholar
  94. Wallis, I. R., Edwards, M. J., Windley, H., Krockenberger, A. K., Felton, A., et al. (2012). Food for folivores: Nutritional explanations linking diets to population density. Oecologia, 169, 281–291.CrossRefPubMedGoogle Scholar
  95. Warren, Y., Higham, J. P., MacLarnon, A. M., & Ross, C. (2011). Crop-raiding and commensalism in olive baboons: The costs and benefits of living with humans. In V. Sommer & C. Ross (Eds.), Primates of Gashaka (pp. 359–384). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.Google Scholar
  96. Watts, D. P., Potts, K. B., Lwanga, J. S., & Mitani, J. C. (2012). Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 1. Diet composition and diversity. American Journal of Primatology, 74, 114–129.CrossRefPubMedGoogle Scholar
  97. Weyher, A. H., Ross, C., & Semple, S. (2006). Gastrointestinal parasites in crop raiding and wild foraging Papio anubis in Nigeria. International Journal of Primatology, 27, 1519–1534.CrossRefGoogle Scholar
  98. Wrangham, R. W., & Waterman, P. G. (1983). Condensed tannins in fruits eaten by chimpanzees. Biotropica, 15, 217–222.CrossRefGoogle Scholar
  99. Wrangham, R. W., Conklin, N. L., Chapman, C. A., & Hunt, K. D. (1991). The significance of fibrous foods for Kibale Forest chimpanzees. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 334, 171–178.CrossRefPubMedGoogle Scholar
  100. Wrangham, R. W., Conklin-Brittain, N. L., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. International Journal of Primatology, 19, 949–970.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Anthropology Centre for Conservation, Environment and DevelopmentOxford Brookes UniversityOxfordUK
  2. 2.Zoological Institute, Animal Ecology & ConservationUniversität HamburgHamburgGermany

Personalised recommendations