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A fundamental issue in ecology is determining factors that regulate animal abundance. A variety of potential factors have been proposed, including external factors such as food resources, weather, predation and disease, and internal conditions such as territoriality and aggressive behaviours (Krebs 1978; Boutin 1990). The importance of understanding determinants of animal abundance has become increasingly vital as ecologists are asked to apply their knowledge to develop informed management plans for endangered or threatened species. However, understanding and predicting factors that determine the abundance of particular species have proven extremely difficult, and thus there are few general hypotheses addressing this topic. Studies of folivorous primates are a notable exception. Milton (1979) proposed that year-round availability of digestible mature leaves, which are used by colobus monkeys when other more preferred foods are unavailable, limits colobine populations (see also McKey 1978). Therefore, if easily digestible mature leaves are plentiful in an area when other more preferred foods are lacking, the site may support a relatively large population of colobines (Davies 1994). By measuring overall mature leaf quality as the ratio of protein to fibre, several subsequent studies have found positive correlations between colobine biomass and this index of leaf quality (Waterman et al. 1988; Oates et al. 1990; Chapman et al. 2002). A similar relationship was also found for some folivorous lemurs of Madagascar (Ganzhorn 1992).
Each primate species has a protein threshold below which it cannot maintain bodily functions (Milton 1979; Milton, van Soest & Robertson 1980). As for fibre, there is substantial evidence that colobines can digest some fibre components, but not lignin (Waterman & Choo 1981; Waterman & Kool 1994). Thus, increasing fibre content increases the amount of food ingested that cannot be digested and slows the rate of passage of digesta through the stomach. This reduces the efficiency of bacterial enzyme action, causing a reduction in protein uptake (Milton 1979, 1982, 1998).
While correlative studies suggest that the protein to fibre ratio of available foods may limit colobine populations, there are reasons to be sceptical. This scepticism is based on a number of factors. First, there is controversy over the importance of protein to primates. Oftedal (1991) calculated that even a primate population with low protein digestibility caused by consumption of tannin would require only 7–11% protein on a dry matter basis (DM) for growth and maintenance, and only 14% (DM) for reproduction (note that the impact of tannins on digestibility is not well understood; Mole & Waterman 1985; Waterman & Kool 1994). Because leaves eaten by primates average 12–16% (DM) protein (Glander 1982), Oftedal concluded that it is unlikely that protein deficiency will be a problem for most primates, except for lactating females eating a diet high in tannins. With respect to colobines, protein demand might be even lower, because blood urea can be recycled by secreting it into saliva or diffusing it across the wall of the foregut. This nitrogen source can then be used by microbes for protein synthesis, and the microbes are digested in turn in the small intestine (Kay & Davies 1994).
Finally, scepticism towards the protein to fibre model is warranted because all the studies to date are correlative and based on small sample sizes (i.e. < 12). Some other characteristic of the folivores’ foods, that is correlated with protein but not yet identified, may be responsible for maintaining their populations. Along these lines, researchers have often considered the energy content of foods to play a critical role in diet selection (Schoener 1971). Dasilva (1992, 1994) presented evidence that a population of Colobus polykomos (Zimmerman) on Tiwai Island, Sierra Leone, was limited seasonally by the availability of energy-rich foods and did not select foods based on protein content. Furthermore, seeds, which had the highest energy content of all parts consumed, were the most preferred food type for this population. Dasilva's findings run counter to the observation that colobine biomass can be predicted by the protein to fibre ratios in mature leaves and suggest that energy may play a crucial role in colobine nutritional ecology.
Given this controversy, and Dasilva's findings for C. polykomos, the objective of this study was to evaluate the importance of food energy content to the red colobus Procolobus badius (Kerr) and black-and-white colobus monkeys C. guereza (Rüppell) of Kibale National Park, Uganda. We took three approaches. First, we examined if these two colobus monkeys were selecting foods with high energy content and determined if the protein to fibre ratio of their foods was correlated with energy content. This analysis was conducted on eight groups living in different ecological settings and involved over 3000 h of observations conducted over 2 years. Groups were selected to maximize the chances of obtaining variation in the intensity of feeding competition. Thus, groups varied in size (large groups are expected to experience more feeding competition than small) and level of disturbance (groups in more disturbed habitats are expected to experience greater feeding competition). Secondly, to provide a crude evaluation of whether or not the study groups were expending more energy than they were obtaining, we mimicked the analysis of Dasilva (1992), with a few adjustments allowing for a more accurate estimate. This analysis produced rough approximations of energy expenditure and consumption for males and non-reproductive, lactating and pregnant females of each group. Finally, we examined the relationship between colobus biomass and food energy content across four populations representing a range of both biomass and energy availability. This was conducted following the methods used to test the protein/fibre model (Oates et al. 1990); the energy content of mature leaves of the 20 most common plants in each habitat were quantified and related to colobine biomass.
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Both species relied most heavily on young leaves regardless of group size or ecological setting (Table 1). The importance of other plant parts in the diets of the two colobus species in the different areas was highly variable. Mature leaves were eaten frequently by groups of both species in the forest fragment. Interestingly, the black-and-white colobus in the fragment ate ripe fruit for almost 10% of their foraging time. In general, young leaves and flowers had high levels of protein and little fibre; however, there was considerable variation among species (Table 2). For example, the protein to fibre ratio of young leaves ranged from a low of 19 for Parinari excelsa to 303 for Celtis durandii, whereas the mean for all species eaten by the colobus was 139. As might be expected, fruit (average = 22·4 kJ/g (OM), SD = 1·8) and flowers (22·4 kJ/g (OM), n = 1) tended to have a high energy content, although considerable interspecific variation was found in the energy content of the fruit (Table 2). Overall, the energy content of the colobus foods ranged from 18·0 kJ/g (OM) (Eucalyptus bark) to 24·4 kJ/g (OM) (Prunus africana ripe fruits).
Table 1. The percentage of total feeding observations that different colobus groups in or near Kibale National Park, Uganda spent eating different plant parts (leaf buds are included in young leaves)
| ||Ripe fruit||Unripe fruit||Flowers||Young leaves||Mature leaves||Petioles||Bark|
| Big||5·0||1·6||3·5||75·6|| 5·6||7·9||0·3|
| Mikana||2·7||2·9||1·8||78·5|| 7·4||5·8||0·2|
| Big||0·0||0·0||2·2||84·4|| 3·6||0·8||0·0|
| Small||2·4||7·2||0||77·7|| 5·8||0·4||4·8|
| Mikana||1·8||8·1||3·4||78·2|| 5·3||3·1||0·1|
| Average||3·4||4·5||3·0||76·3|| 7·2||1·3||1·4|
Table 2. The average, standard deviation and sample size of the protein, fibre, and energy content (OM − organic matter basis; DM − dry matter basis) for different plant parts eaten by the colobus monkeys of Kibale National Park, Uganda
| ||Sample size||Protein/fibre||Energy (OM)*||Energy (DM)*|
|Mature leaves||13|| 88·30||55·30||21·4||0·60||19·5||0·94|
|Petioles|| 5|| 33·50|| 9·30||18·8||0·37||16·5||0·58|
|Ripe fruit|| 3|| 33·00||16·00||22·4||1·82||21·0||1·30|
|Bark|| 2|| 7·01|| 0·71||18·0||0·21||15·9||0·54|
|Unripe fruit|| 1|| 15·70|| ||23·0|| ||21·2|| |
|Flowers|| 1||184·00|| ||22·4|| ||20·4|| |
Neither red nor black-and-white colobus selected foods that were high in energy: all eight groups showed no correlation between energy content of their foods and foraging effort (P > 0·263 for all groups). In contrast, the protein to fibre ratio was correlated with foraging effort for both red and black-and-white colobus in seven of the eight groups (P < 0·05; the group with no correlation was the small group of red colobus from forestry compartment K-30).
When the availability of the different species of food plants were controlled statistically, again seven of the eight groups showed evidence of selection for foods high in protein and low in fibre, as indicated by a significant partial correlation coefficient (P < 0·05). Only the small red colobus group from K-30 showed no evidence of selecting foods high in protein and low in fibre after controlling for food availability. When the availability of the different species of food plants was removed statistically, again there was no evidence that any of the groups selected foods that were high in energy (P > 0·442).
The energy content of the foods of the colobus monkeys was not correlated with their protein content (P = 0·108, n = 43) or the protein to fibre ratio (P = 0·357, n = 43).
Calculating an index of activity as the amount of time the groups were active (feeding, travelling, grooming) minus the amount of time inactive (resting) illustrates marked variation, with the largest difference being 41·7% (Fig. 1). Black-and-white colobus were more inactive than red colobus, and groups in disturbed areas were more inactive than groups in undisturbed habitats.
Figure 1. The level of activity (proportion of time spent active (feeding, travelling, etc.) minus the amount of time spent inactive during the (day) for eight groups of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) living in or near Kibale National Park Uganda (Uganda RCBig − the large group of red colobus at Kanyawara, RCSmall − the small group of red colobus at Kanyawara, RCMik − the group of red colobus in the logged area known as Mikana, RCNk − the red colobus group at Crater Lake Nkuruba; BWBig − the large group of red colobus at Kanyawara, BWSmall − the small group of red colobus at Kanyawara, BWMik − the group of red colobus in the logged area known as Mikana, BWNk − the red colobus group at Crater Lake Nkuruba).
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When comparing both estimates of energy expenditure (DEE and ADMN) to estimates of energy consumption (85% availability), none of the groups are found to be energy deficient (Table 3). Furthermore, for the red colobus, no age/sex class in any group was found to be energy deficient unless digestive efficiency was so low that only 19% of ingested energy was available when comparing to ADMN and 27% or less availability when comparing to DEE. The first age/sex class red colobus to be energy deficient in these cases are the males from the Mikana group. For the black-and-white colobus, a 60% or less availability value must be assumed when comparing ADMN and 33% or less availability value must be assumed with DEE to find an instance of energy deficiency. Such low estimates of availability seem unrealistic, given current studies (Watkins et al. 1985); therefore, these two colobus species do not appear to be energy deficient.
Table 3. Rough estimates of the energy expenditure (daily energy expenditure (DEE) and average daily metabolic needs (ADMN)) and consumption (with 85% availability of ingested energy assumed) for four groups of red colobus and four groups of black-and-white colobus monkeys found in or near Kibale National Park, Uganda. All values in kJ/day
|Species||Sex||BMR||DEE||ADMN*||Energy consumed**||Energy available**|
|Procolobus badius1||Female|| 797||1593||1242||13935||11845|
| ||Pregnant|| 996||1992||1375||13935||11845|
|Procolobus badius2||Female|| 797||1593||1225||11939||10148|
| ||Pregnant|| 996||1992||1360||11939||10148|
|Procolobus badius3||Female|| 797||1593||1232||11009|| 9358|
| ||Lactating||1195||2390||1500||11009|| 9358|
| ||Pregnant|| 996||1992||1366||11009|| 9358|
| ||Male||1442||2884||2054||11009|| 9358|
|Procolobus badius4||Female|| 797||1593||1196||13084||11121|
| ||Pregnant|| 996||1992||1336||13084||11121|
|Colobus guereza1||Female||1270||2541||1734|| 7199|| 6120|
| ||Lactating||1906||3811||2202|| 7199|| 6120|
| ||Pregnant||1588||3176||1968|| 7199|| 6120|
| ||Male||1621||3241||2151|| 7199|| 6120|
|Colobus guereza2||Female||1270||2541||1715|| 6725|| 5716|
| ||Lactating||1906||3811||2190|| 6725|| 5716|
| ||Pregnant||1588||3176||1952|| 6725|| 5716|
| ||Male||1621||3241||2128|| 6725|| 5716|
|Colobus guereza3||Female||1270||2541||1688|| 8099|| 6884|
| ||Lactating||1906||3811||2174|| 8099|| 6884|
| ||Pregnant||1588||3176||1931|| 8099|| 6884|
| ||Male||1621||3241||2099|| 8099|| 6884|
|Colobus guereza4||Female||1270||2541||1681|| 9732|| 8272|
| ||Lactating||1906||3811||2170|| 9732|| 8272|
| ||Pregnant||1588||3176||1926|| 9732|| 8272|
| ||Male||1621||3241||2090|| 9732|| 8272|
Colobine biomass at the four sites within Kibale varied from 191 kg/km2 at the Dura River to 2675 kg/km2 at Mainaro in Kibale (mean biomass across sites = 1316 kg/km2). As demonstrated previously (Chapman et al. 2002), colobine biomass appears to be related to the average protein to fibre ratio of mature leaves from the 20 most abundant tree species at each site (Fig. 2a). In contrast, there is no evidence that the biomass at these sites is related to the energy content of mature leaves from the 20 most abundant tree species at these sites (Fig. 2b).
Figure 2. The relationship between (a) the average protein to fibre ratio and (b) the energy content of the mature leaves from the 20 most abundant tree species at four sites in Kibale National Park, Uganda, and the biomass of red colobus and black-and-white colobus at those sites.
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Three lines of evidence suggest that neither of the colobine species we studied were limited by energy availability; (1) they did not select food based on energy content; (2) crude estimation of energy gain vs. expenditure suggested that energy was not limiting; and (3) the biomass of colobus at the four sites in Kibale was not related to the energy content of the available mature leaves. In contrast, seven of eight groups preferred foods that were high in protein and low in fibre, and biomass of colobines could be predicted based on the protein to fibre ratios of the available mature leaves.
These results provide support for Milton's (1979) protein to fibre model, but do not provide evidence to support Dasilva's (1992) suggestion that the colobus monkeys generally suffer from shortages of high energy foods. Why the conclusions of Dasilva's and this study differ is not readily apparent. It may be that the Tiwai Island population of colobus that Dasilva studied had sufficient protein available to them in the seeds they selected (Dasilva 1992), so the need for energy took precedence in limiting population size. However, this is not supported by the observation that the colobus biomass at the Tiwai Island site is relatively low (Oates et al. 1990), and it runs counter to the widespread application of the protein to fibre model to account for variation in colobus biomass in Africa (including Tiwai) and South-east Asia (Oates et al. 1990). A methodological point worth mentioning is that Harvey & Clutton-Brock's (1981) equation that Dasilva used employs an estimate of basal metabolic rate that is high relative to the actual rate documented by Müller et al. (1983) for C. guereza. This will overestimate the average daily metabolic needs, as well as DEE, and may therefore suggest energy deficiency when not actually the case. However, it is unlikely that this completely explains the differences among these studies. It may be that our populations of colobus monkeys were able to behaviourally respond to periods when energy was scarce and thus effectively avoid any need to select high energy foods. This idea is supported by the fact that we documented large differences in activity levels among groups. In general, the groups that we would have expected to be experiencing more intense feeding competition (i.e. those groups in the logged area or the forest fragments) tended to be more inactive, potentially conserving energy. If, at times when high energy foods were difficult to find, the groups could easily find foods high in protein and low in fibre without incurring high travel costs, the animals could decrease activity, and thus need not be concerned about the energy content of their foods. The differences between our study and that of Dasilva do highlight the importance of quantifying and understanding factors that may underlie differences in activity patterns (see also Dasilva 1992).
Milton (1979) suggested that for small mammalian herbivores, the protein to fibre ratio may be a good predictor of leaf choice. McKey (1978) proposed that year-round availability of digestible mature leaves, which are used by colobus monkeys when other more preferred foods are unavailable, limits the size of colobine populations. In this study we found that for seven of the eight groups observed, the protein to fibre ratio was a good predictor of food choice. However, we have been collecting quantitative data on colobus foraging in Kibale since 1992, involving over 6000 h of observations. During this time, we have never observed groups to eat mature leaves for extended periods of time (i.e. exclusively for up to a week), as would be suggested if they were a fallback food. Rather, they tend to eat mature leaves during short feeding sessions, typically less than an hour, that occur at widely separated intervals. It may be that we have simply not observed these groups for long enough and that at some time in the future there will be a period when the animals must rely on mature leaves, and such rare events determine the biomass of an area. However, it is also possible that for our populations mature leaves are not ‘fallback’ foods, eaten when other more preferred foods are unavailable. Following Milton (1979), we suggest that the protein to fibre ratio is a good predictor of food choice in small mammalian herbivores. We suggest that areas that generally have food items that are low in fibre and high in protein are able to support high biomasses of these consumers. Thus, it is not the actual protein to fibre ratio of the mature leaves that is important in influencing biomass, but rather the general availability of high-protein, low-fibre foods. Measuring the mature leaves’ protein to fibre ratio may be useful if it correlates with the general availability of high-protein, low-fibre foods.
The influence of the protein to fibre ratio on animal abundance will probably extend beyond the folivorous primates, to include other small mammalian herbivores. Its importance stems from a major problem facing herbivorous animals, the ingestion of long-chain structural polymers that are not hydrolysed easily (McNab 2002). Furthermore, this problem is magnified by size because gut retention time is equivalent to approximately m0·25, where m = body mass (McNab 2002). Thus, smaller species have a shorter retention time, causing greater difficulty in meeting nutritional requirements while ingesting relatively high amounts of fibre. Cork (1994) set a size cut-off for fibre tolerance at 15 kg, below which animals become ‘fibre-intolerant’. Because of this intolerance, the availability of high-quality foods (low fibre, high nutritional value) becomes ever more important to the health of small herbivores. In our study, we have demonstrated further the importance of protein over other nutritional characters, thereby further defining high-quality folivorous foods as low-fibre, high-protein. With a high-quality folivorous diet possibly being more difficult to obtain or the need for physiological adaptations (i.e. fore-gut fermentation) to deal with fibre, there are few folivores falling under a 15 kg threshold: mainly sloths, primates, hares, rabbits, voles and lemmings (McNab 2002). The abundances of these small folivores are probably the most heavily influenced by the protein to fibre model.
In addition, other small herbivorous mammals may potentially be influenced by this ratio. Studies show that various herbivores select foods high in protein and low in fibre. In the agile wallaby (Macropus agilis) (Gould), a shift in diet occurs from the wet to dry season in response to preferred foods having lower protein and digestibility (higher fibre) in the dry season (Stirrat 2002). Others describe behavioural mechanisms allowing for the ingestion of more protein and less fibre. For example, Lowry (1989) found that the black fruit bat (Pteropus alecto) (Temminck) chews the leaves of the tree Albizia lebbek (Linnaeus), swallows the liquid extract (which is 36% protein) and spits out the fibrous residue, thus increasing protein and decreasing fibre consumption.
In general, this study provides support for the notion that the protein to fibre ratio is a good predictor of food choice in colobines and for the use of this index of food quality in predicting colobine biomass. The importance of understanding determinants of animal abundance has become increasingly vital, as ecologists are asked to apply their knowledge to develop informed management plans for endangered or threatened species (Chapman & Peres 2001). This study provides support for the use of the protein to fibre model in the conservation and management of colobines, by showing that general food preference is influenced by the protein to fibre ratio, and by finding no evidence to support the alternative hypothesis that colobines are limited by availability of high energy foods. This information could be used by managers in a number of ways. For example, if important food trees used by colobines could be left standing in selective logging operations or if loggers could use directional felling to reduce impact to these trees, for primate species that are negatively impacted by logging their population decline might be less severe or the speed of population recovery might be improved. The results of this study suggest that the tree species targeted for such treatment should provide food items with a high protein to fibre ratio. Energy availability does not appear to be of significant concern in the conservation of black-and-white colobus and red colobus monkeys.
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Funding for this research was provided by the Wildlife Conservation Society and National Science Foundation (grant number SBR-9617664, SBR-990899) and Michael Wasserman was supported by an REU Supplement and the University Scholars Program at the University of Florida. Permission to conduct this research was given by the Office of the President, Uganda, the National Council for Science and Technology and the Uganda Wildlife Authority. We would like to thank Tom Gillespie and Sophia Balcomb for help with the census work, Karen Bjorndal, Alan Bolten, Matt Burgess, Peter Eliazar, Erin Hauck, Raime Fronstin, Kate Moran and Ada Mayte Santamaria for help with nutritional analysis, Glynn Davies for interesting discussions about protein and energy and Lauren Chapman, Brian McNab, Katie Milton and Sue Boinski for helpful comments on this project.