Journal of Undergraduate Research
Volume 4, Issue 1 - September 2002

Colobus Diet Selection and Abundance: The Role of Energy and the Protein to Fiber Ratio

Michael Wasserman

ABSTRACT

Understanding the nutritional ecology of a species is crucial knowledge for maintaining healthy populations or conserving endangered populations. Two specific nutritional characteristics thought to be important to colobus monkeys are the energy content and protein to fiber ratio of their foods. The objective of this project was to examine how the energy content and the protein to fiber ratio of various plant species and parts affected the diet selection and abundance of two species of colobus monkeys (Procolobus badius and Colobus guereza) found in Kibale National Park, Uganda. This was done by analyzing the relationship between these two nutritional characteristics and colobus foraging effort for the various plant species consumed, as well as examining the relationship between the average energy availability and colobine biomass of four sites within Kibale. It was found that while the energy content was not correlated with diet selection, the protein to fiber ratio was correlated for five out of the eight groups studied. Additionally, energy content and the protein to fiber ratio were not significantly correlated. Finally, biomass was not influenced by energy availability. This project demonstrates that energy availability is of no concern in the conservation of these species, but supports the application of the protein to fiber model for the management of endangered colobus monkeys.

INTRODUCTION

Understanding the nutritional ecology of a species is crucial knowledge for maintaining healthy populations or conserving endangered populations. For example, an understanding of the specific nutrients that a species struggles to obtain can be used if selective logging must take place, in that efforts can be made to preserve those plants that are high in the critical nutrients (1). This concern is particularly relevant to the folivorous red colobus monkey (Procolobus badius), as their populations have been found to decline by 44% when comparing unlogged forest to heavily logged forest (2).

The red and black-and-white colobus monkeys (Colobus guereza) are members of the Colobinae subfamily, a group commonly known as the leaf-eating monkeys. In all populations of red colobus studied to date, young leaves are the most commonly eaten food item. Some populations of black-and-white colobus monkeys also rely heavily on young leaves; however, others eat significant quantities of seeds. One hypothesis for the preference for young leaves suggests that they are selecting for their protein content (1). Nutritional analysis has supported this, as young leaves of the commonly eaten Celtis durandii have twice as much protein as mature leaves (3). Further research has shown the protein to fiber ratio of available foods is an important determinant of colobine abundance (4).

However, it has also been suggested that protein is not limiting in most primate populations (5). Additionally, since colobines receive protein via microbial activity in the gut, their protein demand might be even lower than most primates (6). Furthermore, Dasilva found that a population of Colobus polykomos was energy deficient at certain times of the year and did not select food based on their protein content (7-8). Consequently, Dasilva suggested that energy content was an important factor in diet selection. Supporting this, seeds were the most preferred food type and also had the highest energy content of all plant parts consumed (7). Nonetheless, it remains unclear as to whether the protein or energy content of colobus foods is most regulating their populations.

In this study, the importance of the availability of energy to the red colobus and black-and-white colobus monkeys in Kibale National Park, Uganda was considered.The objective was to examine how the energy content of colobus foods affected their abundance, and how this related to previous findings suggesting that the protein to fiber ratio of their foods is of primary importance. This was accomplished by addressing two main questions. First, I determined if the colobus monkeys showed a diet selection in favor of high energy foods using behavioral observations of eight groups involving more than 3000 hours of observation. Additionally, the possibility of a confounding effect due to selection for high protein to fiber foods was addressed. Secondly, direct tests of the idea that colobus are energy limited were made by relating colobus biomass to energy availability at four sites within Kibale.

METHODS

Determination of Energy Content

Plant material of the various species eaten by the red and black-and-white colobus monkeys, as well as leaves from the 20 most abundant tree species at four different sites, was collected according to species and part in Kibale National Forest, Uganda (see (1) for detailed information on the collection procedure; see (9) for a description of the study site). These samples were dried, placed in plastic storage bags, and brought back to the University of Florida. They were then ground into a fine powder using a Wiley Mill (1 mm mesh screen) and a coffee grinder.

Using the powder formed, the energy content of various plant parts was determined using a Parr Oxygen Bomb Calorimeter, following standard procedures (10-11). With the data collected, along with the percent dry matter and organic matter of the sample and the calibration value for the specific bomb, the energy content (J/g) on an ash-free organic matter basis was calculated.

Data on the protein and fiber content of the various plant species/parts were provided by Colin Chapman.

Behavioral Observations

The foraging behavior of four groups of red colobus and four of black-and-white colobus was studied at Kibale. The behavioral data were supplied by Colin Chapman. Based on this, foraging effort was calculated for each group as the number of times seen feeding on a particular plant species and part (e.g., leaf petioles of Markhamia platycalyx) divided by the total observations of feeding on all species and parts. This variable was used to represent diet selection.

Analyses

To evaluate if the different species/groups were selecting food items that were high in energy or which had a large protein to fiber ratio, a Pearson's correlation test was run to determine the relationship between these nutritional values for each plant species and part and the colobus foraging effort for that particular food. Furthermore, a correlation test was run to determine if a relationship between energy content and the protein to fiber ratio or protein content existed.

To examine if the energy content of the foods could limit the size of colobine populations, I examined the relationship between colobine biomass values (provided by Colin Chapman) and the average energy content of mature leaves of the 20 most abundant tree species at each of the four sites. A similar examination was made for the protein to fiber ratio.

RESULTS

Both species fed mostly on young leaves; 69% of the red colobus's foraging effort and 76% of the black-and-white colobus's foraging effort was concentrated on this food type. They also both fed on petioles, mature leaves, ripe fruits, unripe fruits, flowers, buds, and bark. Red colobus rarely fed on seeds (Table 1).

The energy content of the colobus foods ranged from 18000.14 J/g (OM) (Eucalyptus bark) to 24440.04 J/g (OM) (Prunus africana ripe fruits). Ripe fruits had the most energy (average = 22437 J/g (OM), S.D. = 1820), while bark had the least (average = 18000 J/g (OM), S.D. = 213) (Table 2).

Selection for energy did not occur in either red or black-and-white colobus foraging, as all 8 groups showed no correlation between energy and foraging effort (p > 0.445, n = 43 for all groups). Energy content was not correlated with protein content (p = 0.108, n =43) or the protein to fiber ratio (p = 0.357, n = 43). In contrast, the protein to fiber ratio was correlated with foraging effort for red and black-and-white colobus in five of the eight groups (p < 0.05, n = 43).

As previously demonstrated (4), colobine biomass was correlated to the average protein to fiber ratio of mature leaves from the 20 most abundant tree species at each site (r = 0.945, p = 0.055, n = 4; Figure 1a). In contrast, there was no evidence that the biomass at these sites was correlated to the energy content of mature leaves from the 20 most abundant tree species (r = -0.151, p = 0.849, n = 4; Figure 1b). It should be noted that with such a small sample size, the scope of the biomass results are limited.

Figure 1 a,b. The relationship between the average protein to fiber ratio (a) and energy content (b) of the mature leaves from the 20 most abundant tree sites at 4 sites in Kibale National Park, Uganda, and the biomass of red colobus and black-and-white colobus at those sites.

DISCUSSION

The importance of the protein to fiber ratio as a determinant of colobine abundance has been outlined through numerous studies. It has been suggested that year-round availability of digestible mature leaves, which are used by colobus monkeys when other more preferred foods are unavailable, limits colobine abundance (12-13). If easily digestible mature leaves are abundant during famine periods, the site can support a larger population of colobines. Defining digestibility as the ratio of protein to fiber, several subsequent studies found positive correlations between Asian and African colobine biomass and this nutritional quality (14). Furthermore, it has been recently shown that red colobus in Kibale select foods high in protein and low in fiber (1).

This study further supports these conclusions since it suggests that the colobus monkey groups were not selecting food based on their energy content and energy was not a determinant of colobine biomass. These findings conflict with ideas about the importance of energy for colobus monkeys proposed by Dasilva (7). As for the confounding effects between energy content and the protein to fiber ratio, the data do not support any need for concern. Therefore, I suggest that the protein to fiber ratio of colobus foods is of utmost importance in determining the health of their populations and that the protein to fiber model should be incorporated into management practices directed towards endangered colobus monkeys. The availability of energy does not appear to be of significant concern in the conservation of these species.

REFERENCES

1. Chapman, C.A. and L.J. Chapman. Foraging challenges of red colobus monkeys: Influence of nutrients and secondary compounds. Comparative Biochemistry and Physiology (In Press).
   
2. Chapman, C.A., S.R. Balcomb, T.R. Gillespie, J.P. Skorupa, and T.T. Struhsaker. 2000. Long-term effects of logging on African primate communities: a 28-year comparison from Kibale National Park, Uganda. Conservation Biology 14:207-217.
   
3. Struhsaker, T.T. 1975. The Red Colobus Monkey. University of Chicago Press, Chicago.
   
4. Chapman, C.A., L.J. Chapman, K.A. Bjorndal, and D.A. Onderdonk. 2002. Application of protein to fiber ratios to predict colobine abundance on different spatial scales. International Journal of Primatology 23:283-310.
   
5. Oftedal, O.T. 1991. The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Philosophical Transactions of the Royal Society London B 334:161-170.
   
6. Kay, R.F. and G. Davies. 1994. Digestive physiology. In Davies, A.G. and J.F. Oates (eds.). Colobine Monkeys. Cambridge University Press, Cambridge, pp 229-249.
   
7. Dasilva, G.L. 1992. The western black-and-white colobus as a low-energy strategists: Activity budget, energy expenditure and energy intake. Journal of Animal Ecology 61:79-91.
   
8. Dasilva, G.L. 1994. Diet of Colobus polykomos on Tiwai Island: Selection of food in relation to its seasonal abundance and nutritional quality. International Journal of Primatology 15:1-26.
   
9. Chapman, C.A. and J.E. Lambert. 2000. Habitat Alteration and the conservation of African primates: Case study of Kibale National Park, Uganda. American Journal of Primatology 50: 169-185.
   
10. Parr Instrument Company bomb calorimetry manuals.
    
11. Paine, R.T. 1971. The measurement and applications of the calorie to ecological problems. Annual Review of Ecology and Systematics 2: 145-164.
    
12. McKey, D.B. 1978. Soils, vegetation, and seed-eating by black colobus monkeys. In Montgomery, G.G. (ed.). The Ecology of Arboreal Folivores. Smithsonian Institution Press, Washington, DC. pp 423-437.
    
13. Milton, K. 1979. Factors influencing leaf choice by howler monkeys: A test of some hypotheses of food selection by generalist herbivores. American Naturalist 114:363-378.
    
14. Oates, J.F., Whitesides, G.H., Davies, A.G., Waterman, P.G., Green, S.M., Dasilva, G.L., and Mole, S. 1990. Determinants of variation in tropical forest primate biomass: New evidence from West Africa. Ecology 71:328-343.

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