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International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
International Journal of Primatology, Vol. 24, No. 3, June 2003 ( C© 2003)
Mineral Resource Availability and Consumptionby Colobus in Kibale National Park, Uganda
Karyn D. Rode,1 Colin A. Chapman,1,2,∗ Lauren J. Chapman,1,2
and Lee R. McDowell3
Received July, 11, 2002; revision October 28, 2002; accepted November 11, 2002
Very little information exists on mineral nutrition of tropical, forest-dwellingspecies, yet minerals are critical to growth, reproduction, and survival. Weexamined the mineral resources available to and consumed by colobus inKibale National Park, Uganda. We combined behavioral data on black-and-white (Colobus guereza) and red colobus (Piliocolobus tephrosceles) in asection of unlogged forest, a heavily logged area, and a forest fragment withmineral analysis of their foods to estimate the proportion of the diet containingspecific minerals (mineral content). We compared mineral content of colobusfoods (natural and crops) across plant parts and among plant species. Addi-tionally, we estimated mineral intake of frugivorous primates in Kibale frompublished dietary data and our estimates of mineral content of foods. Dietarymineral content for all colobus groups and frugivorous species is similar de-spite significant differences in the mineral content of foods. Ripe and unripefruits are lower in mineral content than most foods. Foods rarely consumed,such as bark, petioles, and caterpillars have high levels of some minerals. Themineral content of crops is low in comparison to that of natural foods. For allcolobus groups of both species, sodium content of foods was extremely lowand iron content was generally low, suggesting that intake is below suggestedrequirements, though current suggested iron requirements may overestimatephysiological needs. Copper content was marginal and deficient seasonallyfor most colobus groups. Despite a sodium-limiting environment, only one of8 colobus groups appeared to select sodium; however, this may be due to a lack
1Department of Zoology, University of Florida, Gainesville, FL 32611.2Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, NY 10460.3Animal Sciences Department, University of Florida, Gainesville, FL 32611.*To whom correspondence should be addressed; e-mail: [email protected].
541
0164-0291/03/0600-0541/0 C© 2003 Plenum Publishing Corporation
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542 Rode, Chapman, Chapman, and McDowell
of variation in sodium content among plant species and a positive correlationbetween high plant sodium content and secondary compounds. Despite thelack of selection for sodium by colobines, some behaviors point to a poten-tial sodium deficiency, including urine drinking, consumption of high-sodiumswamp plants, and use of mud-puddles.
KEY WORDS: colobines; minerals; nutrition; herbivory; crop raiding; foraging; sodium;population regulation.
INTRODUCTION
Mineral resources are critical for physiological function, growth, andreproduction in animals (McDowell, 1992; Robbins, 1993). Because plantsand animals differ in their mineral requirements, herbivores face a difficulttask of identifying and consuming plant species and parts to meet their min-eral requirements. For example, sodium (Na) makes up 90% of total bloodcations and is necessary for muscle contraction, nerve impulse transmission,acid-base balance, and metabolism in animals (Robbins, 1993); however, itis not required by plants, resulting in very low concentrations of sodiumin most plants (Smith, 1976). Due to such discrepancies, mineral deficien-cies are common in herbivores (Bell, 1995; Faber et al., 1993; Fox et al.,2000; Krishnamani and Mahaney, 2000; McDowell, 1992). This is particu-larly true in the tropics, since tropical plants are generally lower in nutri-ents than temperate plants are (Chiy and Phillips, 1995; McDowell, 1985,1997).
Very little is known about the availability and use of minerals by tropi-cal herbivores that feed on canopy trees. In many tropical forests, primatesare the predominant canopy-dwelling herbivore with several species, in-cluding colobines (Colobus spp., Nasalis larvatus), some lemurs (Lemurspp., Hapalemur spp.), and howlers (Alouatta spp.), consuming ca. 100%of their diet as plant parts (Chapman and Chapman, 1999; Silver et al.,2000; Yeager, et al., 1997). They likely face the same challenges of meet-ing mineral requirements as other more commonly studied herbivores, suchas rodents (Weeks and Kirkpatrick, 1978), elephants (Loxodonta africana;Holdo et al. 2002, 1999; Weir, 1972), moose (Alces alces; Belovsky 1981), andother ungulates, e.g., Bison (Bison bison, Delgiudice et al., 1994) and white-tailed deer (Odocoileus virginianus; Hellgren and Pitts, 1997; Ramirez et al.,1996).
Although a few researchers have examined the mineral content of someprimate foods (Oates, 1978; Silver et al., 2000; Yeager et al., 1997), informa-tion on the mineral intake of wild, native primate populations is limited.
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Colobine Mineral Resources 543
This information is important for several reasons. Minerals affect dietarychoices (Laska et al., 2000; Oates, 1978; Power et al., 1999; Yeager et al.,1997), health (Robbins, 1993), home range patterns (McNaughton, 1988),and population densities (McNaughton, 1988; Milewski, 2000; Weeks andKirkpatrick, 1976). Janson and Chapman (2000) list mineral availability asone of 3 factors possibly determining primate population densities, and nu-merous studies suggest that primates select specific plant foods or soils tomeet mineral requirements (Hladik, 1978; Nagy and Milton, 1979; Oates,1978; Yeager et al., 1997). Minerals, particularly calcium (Ca) and Na, areimportant for lactating females, and limitations of them can result in slowergrowth and higher infant mortality (Buss and Cooper, 1970; Power et al.,1999). Literature on humans and domestic animals suggest that mineral de-ficiencies are widespread and lead to disease and reduced growth, immunity,and reproduction (Cunningham-Rundles and Lin, 1998; Hambidge, 2000;Hotz and Brown, 2001; Jackson et al., 2000; Minatel and Carfagnini, 2000;Ruel and Bouis, 1998; Sandstead and Lofgren, 2000). Thus, mineral nutritionin primates probably has direct impacts on population health and viabilityboth via increased susceptibility to disease (Milton, 1996; 1999; 2000) andvia direct effects on condition and reproduction.
Information on nutrient requirements of nonhuman primates is scarce(Kaumanns et al., 2000; Oftedal, 1991), resulting in mineral deficienciesand toxicities in captive primates (Dorrestein et al., 2000; Spelman et al.,1989) and difficulties in accessing habitat quality of wild primates. Exist-ing estimates of nutrient requirements for nonhuman primates are basedon the National Research Council (1978) and Nicolosi and Hunt (1979),but both require updating (Crissey and Pribyl, 1997). National ResearchCouncil (1978) mineral requirements are based on a few species with sim-ple stomachs (Kaumanns et al., 2000) and therefore, are unlikely to reflectthe mineral requirements of all primates, especially those with differing di-gestive morphology, such as colobines. Nicolosi and Hunt (1979) includeda wide safety margin when suggesting mineral requirements for nonhumanprimates, thus the values are likely to be higher than actual requirements(Altmann, 1998).
We examined mineral resources available to and consumed by colobusin Kibale National Park, Uganda. Specifically, our objectives were: 1) to es-timate mineral consumption by red (Piliocolobus tephoosceles) and black-and-white colobus (Colobus guereza) in or near Kibale National Park,Uganda, based on observations in an unlogged forest, a logged area, anda forest fragment, 2) to compare mineral consumption to suggested mineralrequirements for nonhuman primates to evaluate if mineral intake may belimiting, 3) to determine if colobines select for specific minerals, and 4) to
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544 Rode, Chapman, Chapman, and McDowell
compare mineral resource availability and food content for folivorous (asdetermined by our study) and frugivorous primates (based on literature) inKibale National Park.
METHODS
Study Areas
Kibale National Park (766 km2) is located in western Uganda, eastof the Ruwenzori Mountains. Moist semideciduous and evergreen forestmakes up 57% of the park, with grassland (15%), woodland (4%), lakes andwetlands (2%), colonizing forest (19%), and exotic tree plantations (1%)making up the remainder of the park (Chapman and Lambert, 2000). Meanannual rainfall is 1749 mm (1990-2001, or 1547 mm from 1903–2001) and isbimodal in distribution, with peak rainfall occurring from March-May andSeptember-November. September to November rains tend to be heavierthan March-to-May rains. Mean maximum temperature is 23.8◦C, and meanminimum temperature is 15.5◦C (1990-2001; Chapman and Chapman, 1997).
We observed colobus in three areas: the unlogged K-30 forestry com-partment; Mikana, a heavily logged section of forest; and, Nkuruba, a forestfragment outside the park. K-30 is a 282-ha area that has not been com-mercially harvested. However, before 1970, a few large stems (0.03–0.04trees/ha) were removed by pit-sawyers. The tree removal has had little im-pact on forest structure and composition (Skorupa, 1988; Struhsaker, 1997).
Mikana lies in the K-14 forestry compartment. K-14 contains a gradientof light to heavy logging with Mikana located in the heaviest logged portionof the compartment. The extraction in the area used by the study groups isthought to have averaged ca. 21 m3/ha or ca. 7.4 stems/ha. Incidental damagewas high, and it is estimated that ca. 50 % of all trees were destroyed by log-ging and incidental damage (Chapman and Chapman, 1997). Finally, CraterLake Nkuruba (0◦ 32′N and 30◦ 19′E; 9.2-ha forest, 3-ha lake) is an explosioncrater (lake depth mean= 16 m, maximum= 38 m; Chapman et al., 1998), atthe northern end of the Kasenda cluster of ca. 40 crater lakes (Melack, 1978).Being too steep to encourage agriculture, forest remains on the rim of thecrater. In 1991, we initiated a conservation project at the lake to protect thesystem. However, with improved transport in the region, clearing for tim-ber, gin brewing, charcoal, brick making, and agriculture have become moreprofitable; consequently, some neighboring fragments have been cleared(Chapman et al., 2002). As a result, the black-and-white colobus popula-tions have increased by 320% since 1995, likely due to immigration fromcleared fragments.
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Colobine Mineral Resources 545
Behavioral Observations
We followed 2 groups of both red and black-and-white colobus in theunlogged forest and a single group of each species in the heavily logged area,and in the forest fragment. The 2 groups in the unlogged area differed in size(red colobus n = 48 and 24 individuals, black-and-white colobus n = 9 and6 individuals). We made behavioral observations from dawn to dusk for 4days each month from July 1998–June 1999 for all groups in the unloggedforest (ca. 600 h for both species) and from July 1999 to May 2000 for thegroups in the heavily logged area (ca. 374 h), and from August 1999 to April2000 for forest fragment groups (ca. 306 h). Groups from each study areawere clearly identifiable due to unique characteristics of individuals withinthe group. All colobus groups were well habituated, and observers followingthe groups did not appear to disturb them. Differences in the rate with whichobservations were made (observation hours) resulted largely from the factthat the groups in the heavily logged areas and in the forest fragment couldget into areas where the observers could not see them, i.e., areas on the steepsides of the crater lake or in dense vegetation in the heavily logged area.
During each half-hour the observer was with the group, 5-point sampleswere made of different individuals. If it was feeding, we recorded the speciesand plant part, e.g., fruit, young leaf, leaf petiole. Part categories includepetiole, leaf bud, flowers, young leaves, mature leaves, ripe fruit, unripefruit, seeds, and bark. We tried to record activities of both conspicuous andhidden group members.
Habitat Data and Selection
To examine food selection by colobus, we measured tree density inall 4 habitats. We established 12 vegetation transects (200 × 10 m) in theunlogged forest compartment, and established 4 transects in heavily loggedarea (200 × 10 m). In the forest fragment, we established 10 (10 × 60 m)transects around the crater rim from the top of the crater to the bottom.We individually marked each tree>10 cm DBH (diameter at breast height)≤5 m of each side of the trail with a numbered aluminum tag and measured itsDBH. This produced a sample of 1189 trees in the unlogged forest, 270 treesin the logged area, and 267 in the forest fragment.
We calculated selection as the percentage of point samples a group fedon a food item divided by the tree density (# of trees/ha). We observed sometree species to be consumed, but they were not encountered on transectswithin a given habitat. For these species, we assumed there was one treepresent in the habitat, and calculated tree density as 1 divided by the sampledarea.
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546 Rode, Chapman, Chapman, and McDowell
Nutritional Analyses
We collected food items as part of ongoing studies of both colobinespecies and red-tailed monkeys (Cercopithecus ascanius). We present somenon-colobine food items for comparative purposes. We collected all itemswithin one week of the time a primate group consumed them, but they arenot necessarily from the tree in which the monkeys fed. We collected mostitems by cutting branches with a tree pruner. We collected a few fruits oncethey fell to the ground if the canopy was too high to reach branches with a treepruner. We collected caterpillars when red-tailed monkeys were feeding onthem and some fell to the forest floor. We also collected crop foods since pri-mates are common crop raiders (Naughton-Treves, 1998) and motivation forcrop raiding in other species has been attributed to higher mineral contentof crops versus available wild foods (Sukumar, 1990; Sukumar and Gadgil,1988).
We processed food items in a fashion to mimic the feeding behavior ofthe subjects, and we collected only those parts selected by the animals. Forexample, if the monkeys ate leaf petioles, we collected the length of petioletypically consumed. We dried samples in the field either by sun-drying, viaa dehydrator that circulated warm air past the samples, or via a light-bulbheated box with a series of racks. We stored dried samples in sealed plasticbags until they could be transported to the University of Florida for analysis.Samples were dried thoroughly to avoid mold. While drying temperaturewill not influence mineral analyses, it will influence other analyses. As aresult, we assured that the samples were dried <50 C◦ by placing Max/Minthermometers with drying samples. When samples were dried in the dryingoven, the oven was set at its lowest heat setting (37C◦).
We ground all samples in a stainless steel Wiley mill with a 1-mm stain-less steel screen. Preparation for mineral analysis and protocol for analysiswith an atomic absorption spectrophotometer follow procedures outlined byMiles et al. (2001). We determined sample concentrations of each elementby comparing absorbancy to a standard linear regression via 3 standardpoints for each element. We corrected concentrations based on 2 blanksrun per set of 60 samples. Additionally, we ran a sample of known min-eral concentration (Certified National Bureau of Standards Citrus leavesSRM-1572) with each set of samples to ensure that values obtained fromthe atomic absorption spectrophotometer were accurate (NBS, 1982; NIST,1982). We tested 8 minerals for each sample: iron (Fe), copper (Cu), man-ganese (Mn), zinc (Zn), sodium (Na), potassium (K), magnesium (Mg), andcalcium (Ca). We ran multiple samples for most colobus foods and averagedthe results to get a single mineral value for each food item (Appendix 1).However, due to the difficulty of collecting more seasonally and spatially
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Colobine Mineral Resources 547
available foods, such as fruits, only a single analysis could be done on someof them.
It seems valid to combine multiple samples from Mikana and K-30since they are adjacent sites along the same gentle slope. However, the for-est fragment at Crater Lake Nkuruba is 10–12 km from them. Examinationof the soils at the sites (soil pits and cores - Zanne and Chapman unpub-lished data), suggested that there was little variation in soil type over thespatial scale in the region. However, to evaluate if it is valid to use the min-eral content of foods collected in Kibale to represent Nkuruba and viceversa, we collected 17 food items in both areas and contrasted their min-eral content (Cu, Mn, Zn, Fe, Na, Mg, K, Ca) via a paired t-test (paired byspecies). There is no significant difference for any mineral among the twosites.
Determination of Annual and Seasonal Dietary Mineral Content
We assumed the percent of feeding spent—the number of point sampleson that item/all feeding point samples—on a food item to be equal to thepercent contribution of the item to total dry matter intake. This assumptionis probably valid since colobines consume primarily leaves and variation inintake rates and dry matter content between leaf species is relatively low(Rode and Chapman, unpubl. data).
We calculated the mineral content of colobus diets via the average min-eral content for all samples of a single species and plant part collected be-tween August 1998 and July 2001. We used the following formula to deter-mine seasonal and annual average mineral food content—the proportion ofthe diet containing each mineral—for all primate groups:
D min = 6[(%of obs. * min. in food)/100] (1)
where in Dmin is dietary mineral content,6 is the sum for all food items, %of obs. is the percent of time observed feeding on an item, and min. in foodis the parts per million (mg/kg) of a mineral in each food item.
We calculated for each colobus group, the contribution of each item totheir total annual mineral consumption via the following formula:
% contribution = [(% of obs.∗ min. in food)/100]/
ann. min. content∗100% (2)
where in ann. min. content is the annual mineral content. We used this valueto determine the primary sources of minerals in colobus diets.
We compared total mineral content of all colobus groups betweenspecies and between disturbed (Mikana and Nkuruba) and undisturbed
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548 Rode, Chapman, Chapman, and McDowell
habitats (K30). In addition, we compared mineral content to primate re-quirements (National Research Council, 1978; Nicolosi and Hunt, 1979),to requirements for birds, cattle, and other mammals (National ResearchCouncil, 1984; Robbins, 1983), and to total mineral consumption of captiveand semifree-ranging primate groups (Dierenfeld and McCann, 1999; Nagyand Milton, 1979; Oates, 1978; Schwitzer and Kaumanns, 2000). Because cur-rent estimates of primate mineral requirements (National Research Council,1978; Nicolosi and Hunt, 1979) are based on trials of animals with simplestomachs, it is important to compare colobines with other foregut ferment-ing mammals that may have more similar requirements. An updated versionof the National Research Council’s estimates of primate mineral require-ments is soon to be published. We examined seasonal mineral content in theunlogged areas only, since observations there cover 11 mo, while the othergroups were only observed for 9 mo. Our evaluation of whether they havediets that meet requirements should be viewed as tentative given that wedo not have estimates of g dry matter of food eaten per time unit for eachspecies and part. However, if our estimates of the mineral content of foodsare consistently less than mineral requirements, their diet is probably defi-cient in that mineral. Stated another way, if the monkeys spend the majorityof time eating foods low in a particular mineral, intake of that mineral islikely below requirements.
Comparison of Mineral Content by Folivorousand Frugivorous/Omnivorous Primates
We used existing data on food parts consumed by frugivorous/omnivorous primates in Kibale to calculate dietary mineral content and tocompare the values to dietary mineral content of colobus groups. We aver-aged mineral content for all species within a food item category, e.g., youngleaves or fruit, and included foods that were consumed by≥1 of 4 frugivorousprimates (not exclusively the colobus foods listed in Appendix A; N = 57 forripe fruits, 7 for unripe fruits, 15 for seeds, 10 for flowers, 64 for young leaves,5 for pith/stem, and 5 for bark). We used the percentage of each plant partconsumed by chimpanzees (Pan troglodytes), blue monkeys (Cercopithecusmitis), mangabeys (Lophocebus albigena), and red-tailed monkeys (Cerco-pithecus ascanius) from Wrangham et al. (1998) in Equation 1 to estimatedietary mineral content of the frugivorous species. We excluded roots andwood from the diets analyzed because they were not collected. Additionally,Wrangham et al. (1998) did not include insect consumption in dietary anal-yses of the primates; nor did they collect sufficient insect samples to deter-mine their mineral content. Because all diets of frugivorous primate groups
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Colobine Mineral Resources 549
Table I. Foraging effort (% of foraging scans) devoted to different plant parts by redcolobus (RC) and black-and-white colobus (BWC) groups in unlogged forest (largegroup=LG & small group=SG), heavily logged forest (Mikana=Mk), and a Crater Lake
forest fragment (Nkuruba = Nk) in or near Kibale National Park, Uganda
RC BWC
Food Item LG SG Mik Nk LG SG Mik Nk
Ripe fruit 5.0 6.4 2.3 0 0 2.5 0 0.8Unripe fruit 1.6 2.5 0.7 1.9 7.4 6.3 14.3 1.0Flowers 3.5 0.8 2.2 2.3 2.3 0.1 4.1 6.1Young leaves 75.3 62.8 87.0 67.3 86.8 81.0 67.1 71.7Mature leaves 5.6 13.3 2.0 18.4 1.9 4.7 3.6 17.9Petioles 7.9 6.4 4.2 2.8 0.8 0.4 5.9 1.8Leaf buds 0.3 1.3 0.4 0.3 0.6 1.1 4.9 0Bark 0.3 6.4 0 6.4 0 4.0 0.1 0.8Other 0 0 0 0 0.2 0 0 0
had been determined in unlogged and lightly logged habitats, we comparedthem with the diets of the 4 red colobus and black-and-white colobus groups(1 large and 1 small group of each species) that range in similar areas.
Statistical Analyses
We categorized samples into one of 10 food item categories: bark, crops,flowers, ripe fruit, unripe fruit, seeds, petioles, mature leaves, young leaves,and caterpillars. We compared mineral content across categories via a one-way ANOVA with a Scheffe’s post hoc test after testing for normality andhomogeneity of variance. We square-root transformed percentages to ob-tain homogeneity of variances. Although we collected>1000 caterpillars foranalysis, the combined dry weight was sufficient only for 2 mineral analyses.Thus, we omitted caterpillars from statistical comparisons. We comparedmineral content of mature and young leaves from 28 species via a pairedt-test (paired by species). We conducted comparisons of the mineral contentamong species of young leaves from 20 species via a one-way ANOVA.
We conducted partial correlation analysis for all colobus groups to de-termine if food selection is based on any of the 8 minerals when the lineareffects of availability of that food (tree density) are statistically removed.The data are log-transformed.
We used a one-way ANOVA to test whether dietary mineral contentdiffered among red and black-and-white colobus groups, among groups indifferent habitats—unlogged, logged, fragment—and among frugivorous/omnivorous primates and folivorous primates. When necessary, We square-root transformed data to meet the homogeneity of variance assumption.
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550 Rode, Chapman, Chapman, and McDowell
RESULTS
Food Items Consumed by Colobus Groups
For all colobus groups of both species, young leaves were the most com-mon plant part consumed (Table I). For both colobus species, young leavesof Celtis durandii and C. africana ranked in the top 5 foods consumed by allgroups except those in the forest fragment. Celtis durandii was not availablein the forest fragment. For black-and-white colobus groups in unlogged andlogged areas, the 2 tree species were the top 2 species consumed, accountingfor 37–45% of all feeding observations. Red colobus relied less heavily onthem alone and included a variety of other species in their diets, such asDombeya mukole, Parinari excelsa, Prunus africana, and Millettia dura.
Mineral Content of Food Items
Food parts differ significantly in Cu, Mn, Zn, Mg, and Ca (p < 0.001 forall tests, here and below), but not Fe, Na, and K (all non-significant tests p >0.11, here and below; Fig. 1). Crops are significantly lower in most minerals,except K. Cu content is significantly higher in young leaves than matureleaves and higher in flowers than bark and mature leaves. Mature leavescontained significantly higher levels of Mn than those of flowers, petioles,and young leaves. In contrast, ripe fruit contains significantly less Mn thanthose of flowers, petioles, and young leaves. Petioles and flowers containsignificantly higher levels of Zn than those of bark, ripe fruit, and matureleaves. Petioles also contain considerable amounts of Mg (significantly higherthan ripe fruit) and Ca (significantly higher than flowers, ripe fruit, unripefruit, and seeds, and young leaves). Bark contains the highest levels of Ca,significantly higher than in all other foods tested, except petioles. Althoughcaterpillars are not included in statistical tests, they are exceptional sourcesof Cu, Zn, and Fe (Fig. 1).
Paired tests of young leaves and mature leaves from the same treespecies illustrate that young leaves have less ash, and more Cu and Zn thanthose of mature leaves (Table II). A comparison of the mineral content of20 species of young leaves show significant differences among species acrossall minerals (p < 0.01 for all tests). However, differences between speciesare most common for K, Zn, and Cu (Appendix 1).
Less than 50% of all the primate foods are deficient in Mn, Zn, Mg,K, and Ca relative to primate nutritional requirements suggested by theNational Research Council (1978; Appendix 1). However, 60% of the foodsare deficient in Cu, 82% are deficient in Fe, and 100% are deficient in Na.
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Colobine Mineral Resources 551
Fig
.1.C
ompa
riso
nof
mea
nm
iner
alco
ncen
trat
ions
(mg/
kg)
offo
odit
ems
cons
umed
bypr
imat
esin
Kib
ale
Nat
iona
lPar
k,U
gand
a(N=
5(b
ark)
,6
(cro
ps),
10(fl
ower
s),
58(r
ipe
frui
t),
7(u
nrip
efr
uit)
,42
(mat
ure
leav
es),
9(p
etio
les)
,15
(see
ds,
and
64(y
oung
leav
es);
dry
mat
ter
basi
s).
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552 Rode, Chapman, Chapman, and McDowell
Table II. Results of paired t tests of mineral content (mg/kg) in mature and young leaves(N = 28 for all minerals, dry matter basis) consumed by colobines in Kibale National Park,Uganda and comparison with leaves consumed by black howlers (Alouatta pigra) at two
sites in Belize (Silver et al., 2000)
Mature Leaves Young Leaves ML & YL this study
This study Silver et al. This study Silver et al. t p(Mean (± SD)) (2000) (Mean (± SD)) (2000) value value
% Ash 10.1 (± 3.5) 8.4 (± 2.8) −3.71 0.001Cu 7.2 (± 2.9) 11.1 10.2 (± 4.2) 12.7 4.16 0.0003Mn 119.0 (± 100.9) 120.2 154.1 (± 337.8) 160.3 0.53 0.6Zn 17.4 (± 11.5) 20.3 26.8 (± 11.6) 34.3 5.2 <0.0001Fe 137.5 (± 133.6) 123.3 117.1 (± 60.9) 155.4 −0.82 0.42Na 180.4 (± 318.6) 500 149.6 (± 73.0) 1100 −0.5 0.62Mg 2962.7 (± 1236.1) 4200 2676.9 (± 807.7) 3900 −1.25 0.22K 16583.2 (± 6429.4) — 16307.3 (± 5501.3) — −0.19 0.85Ca 10496.6 (± 6086.1) 10700 9990.9 (± 6854.0) 6200 −0.31 0.76
As one might expect, food item contribution to annual mineral con-tent is highest from food items that were consumed the most frequently(Appendix B). Celtis durandii, Celtis africana, Millettia dura, Markhamiaplatycalyx, and Bosqueia phoberos are some of the most frequently con-sumed foods and are also within the top 5 food items contributing to annualmineral content for most minerals. Na is a marked exception, with Eucalyp-tus commonly contributing a large portion of total Na intake for groups withit in their home range.
Seasonal and Annual Content of Minerals
Annual mineral content does not differ between species (Table III,combining groups from all habitats for both species: n = 4 per species, p >0.111 for all minerals except for Zn, p = 0.041) or between disturbed andundisturbed habitats (both species combined compared between disturbedand undisturbed areas; p > 0.30 for all minerals). This analysis should beviewed with caution given that we sampled only 4 groups of each colobinespecies.
It is likely that intake of Mn, Zn, Mg, K, and Ca exceeded require-ments for nonhuman primates suggested by both the National ResearchCouncil (1978) and Nicolosi and Hunt (1979; Table III). Fe and Na intakesare likely deficient for all groups relative to nonhuman primate require-ments and Cu is deficient for 5 of the 8 groups based on National ResearchCouncil (1978) suggestions, but both Cu and Fe are above requirementssuggested by Nicolosi and Hunt (1979). Additionally, Na requirements for
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Colobine Mineral Resources 553
Tabl
eII
I.A
nnua
lm
iner
alco
nten
tby
colo
bine
sin
4ha
bita
tsin
and
arou
ndK
ibal
eN
atio
nal
Par
k,U
gand
a(a
llva
lues
are
inm
g/kg
(dry
mat
ter
basi
s);
num
ber
inpa
rent
hese
sis
%of
requ
irem
ent
met
inth
edi
et;
bold
item
sar
ebe
low
nonh
uman
prim
ate
requ
irem
ents
sugg
este
dby
the
NR
C(1
978)
)
%of
diet
Cu
mg/
kgM
nm
g/kg
Zn
mg/
kgFe
mg/
kgN
am
g/kg
Mg
mg/
kgK
mg/
kgC
am
g/kg
Red
Col
obus
Nku
ruba
68.0
68.
2(8
2)63
.3(1
58)
29.6
(296
)15
2.3
(85)
247.
2(1
2)28
03.4
(107
)17
163.
3(2
15)
1112
9.4
(223
)M
ikan
a95
.33
9.5
(95)
65.8
(165
)29
.7(2
97)
141.
4(7
9)15
5.3
(8)
2480
.2(1
65)
1652
6.5
(207
)97
14.8
(194
)K
30sm
all
79.1
39.
2(9
2)70
.3(1
76)
26.3
(263
)14
3.0
(79)
197.
6(1
0)26
90.2
(179
)15
830.
0(1
98)
1057
3.4
(211
)K
30bi
g90
.510
.1(1
01)
73.5
(184
)30
.6(3
06)
160.
9(8
9)17
3.3
(9)
2752
.3(1
83)
1882
6.6
(235
)10
553.
6(2
11)
Ave
rage
9.2
(92)
68.2
(171
)29
.1(2
90)
149.
4(8
3)19
3.3
(10)
2681
.5(1
79)
1708
6.6
(214
)10
492.
8(2
10)
Bla
ck-&
-whi
teco
lobu
sN
kuru
ba89
.11
8.8
(88)
94.9
(237
)34
.4(3
44)
139.
4(7
7)19
7.9
(10)
2598
.4(1
73)
1710
5.5
(214
)10
574.
6(2
11)
Mik
ana
96.5
310
.5(1
05)
57.5
(144
)36
.4(3
64)
171.
7(9
5)15
8.8
(8)
2561
.3(1
71)
1697
0.4
(212
)99
70.1
(199
)K
30sm
allg
roup
93.1
39.
4(9
4)75
.3(1
88)
29.7
(297
)16
4.0
(91)
233.
0(1
2)25
33.9
(169
)16
304.
6(2
04)
9964
.7(1
99)
K30
larg
egr
oup
94.0
210
.1(1
01)
63.5
(159
)33
.3(3
33)
160.
7(8
9)17
0.0
(8)
2456
.9(1
64)
1775
7.0
(222
)99
14.3
(198
)A
vera
ge9.
7(9
7)72
.8(1
82)
33.5
(335
)15
8.9
(88)
189.
9(9
)25
37.6
(164
)17
034.
4(2
13)
1010
5.9
(202
)R
equi
rem
ents
Non
hum
anpr
imat
es10
3011
196
2000
1600
8000
5400
(NR
C,1
978)
Non
hum
anpr
imat
es2
2020
100
2200
1000
2400
6000
(Nic
olos
iand
Hun
t,19
79)
Cat
tle
(NR
C,1
984)
840
3050
800
1000
6500
2000
–400
0M
ean
inco
mm
erci
alpr
imat
e17
.689
196
492
4000
1800
1050
012
900
diet
s(O
fted
al,1
991)
Req
for
bird
san
dm
amm
alsa
1.6–
63.
7–50
9.2–
3025
–180
500–
2000
300–
1500
2000
–800
040
00–2
5000
(Rob
bins
,199
3)O
ther
Stud
ies
Mac
aca
sile
nus
8.09
106.
4528
.41
85.5
250
028
0038
00(D
iere
nfel
dan
dM
cCan
n,19
99)
Lem
urca
tta13
.59
48.6
35.4
265
.03
800
3500
6300
Col
obus
guer
ezab
(Oat
es,1
978)
2142
4225
240
626
0421
602
1510
6A
loua
ttapa
lliat
a—le
afdi
et6.
850
99.7
956.
932
0010
307.
412
300
(Nag
yan
dM
ilton
,197
9)
aB
irds
and
mam
mal
sin
clud
eph
easa
nts,
quai
l,du
cks,
gees
e,tu
rkey
s,gu
inea
pigs
,ham
ster
s,la
bora
tory
mic
e,no
nhum
anpr
imat
es(e
xcep
tfor
Cu)
and
dom
esti
cra
bbit
s.bC
onsi
dere
da
max
imum
min
eral
inta
keba
sed
on10
0%co
nsum
ptio
nof
aco
mm
on,r
elat
ivel
yhi
ghnu
trie
ntfo
odit
em,C
eltis
dura
ndii.
Not
e.%
ofdi
etis
the
%of
the
food
item
sco
nsum
edth
atw
ere
anal
yzed
for
min
eral
cont
ent.
P1: FYJ
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554 Rode, Chapman, Chapman, and McDowell
cattle are above Na content of colobine foods (National Research Council,1984).
The small and large group of red colobus and black-and-white colobusin the unlogged area of Kibale experienced seasonal variation in mineralcontent (Fig. 2). This resulted from changes in the plant foods eaten at dif-ferent times of the year. Only the large black-and-white colobus group andthe large red colobus group maintained stable intakes of Na throughout theyear. Seasonal highs in Na intake are similar for the small group of both redcolobus and black-and-white colobus peaking in October which correspondsto the peak in seasonal rainfall. Ca, Mn, Cu, Zn, and Fe content are highestfor most groups in October and November, during and immediately afterthe most intense rainy season in Kibale.
Selection of Minerals by Colobines
Both multiple regression analysis between mineral content and selec-tion and partial correlation analyses between mineral content and feedingtime when tree density is held constant, revealed little evidence of selectionbased on mineral content. However, partial correlation analysis suggeststhat the black-and-white colobus group in the heavily logged forest selectedplant parts high in Zn and Na more than expected based on availability, butthey avoided plants with high Cu, Mn, and Fe content (Table IV). The largeblack-and-white colobus group in the unlogged forest also selected plantswith high Zn levels, but avoided plant parts with high levels of Mn and K.
Comparison of Frugivorous/Omnivorous and Folivorous Primates
Estimated mineral content of frugivorous/omnivorous primates inKibale that consume 50–75% of their diet as fruit is similar across species(Table V). In comparison to foods eaten by the colobus, the content of foodseaten by the frugivorous/omnivorous species of Kibale National Park is sig-nificantly lower in Zn, Mg, and Ca and marginally lower in Fe (p < 0.02 forall tests; Table VI).
DISCUSSION
Our study suggests that Na content is low in the foods available to andconsumed by colobus in Kibale National Park. Additionally, Fe and Cu con-tent is marginal relative to suggested requirements for nonhuman primates.
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Colobine Mineral Resources 555
Fig
.2.C
ompa
riso
nof
mon
thly
rain
fall
patt
erns
,sug
gest
edm
iner
alre
quir
emen
ts,a
ndm
iner
alco
nten
tof
4gr
oups
ofco
lobu
sin
Kib
ale
Nat
iona
lPar
k,U
gand
a(o
pen
circ
les=
blac
k-an
d-w
hite
colo
bus–
K30
smal
lgro
up,c
lose
dci
rcle
son
dash
edlin
e=
BW
C-K
30la
rge
grou
p,op
ensq
uare
s=
red
colo
bus-
K30
larg
egr
oup,
clos
edsq
uare
s=R
C-K
30sm
allg
roup
,ope
ntr
iang
les=
catt
lere
quir
emen
ts(N
RC
1984
),cl
osed
circ
les
onso
lidlin
e=
prim
ate
requ
irem
ents
sugg
este
dby
Nic
olos
iand
Hun
t(19
79),
aste
risk
s=
prim
ate
requ
irem
ents
sugg
este
dby
the
Nat
iona
lRes
earc
hC
ounc
il(1
978)
).
P1: FYJ
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556 Rode, Chapman, Chapman, and McDowell
Tabl
eIV
.P
arti
alco
rrel
atio
nan
alys
isbe
twee
nfe
edin
gti
me
onsp
ecifi
cpl
ant
part
san
dm
iner
alco
nten
tw
hen
the
linea
ref
fect
sof
tree
spec
ies
dens
ity
prov
idin
gth
epa
rt(d
ensi
ty=
indi
vidu
als/
ha)
isst
atis
tica
llyre
mov
ed.V
alue
spr
esen
ted
are
prob
abili
tyva
lues
and
thos
ein
pare
nthe
ses
are
corr
elat
onco
effic
ient
s.
RC
BW
C
LG
SGM
ikN
kL
GSG
Mik
Nk
Sam
ple
size
4153
5856
3028
4049
Par
tial
Pro
babi
lity
(par
tial
r)C
oppe
r0.
253
(−0.
202)
0.25
9(−
0.17
0)0.
318
(−0.
143)
0.48
9(-
0.10
1)0.
071
(−0.
383)
0.24
9(−
0.26
3)0.
021∗
(−0.
400)
0.54
6(0
.096
)M
anga
nese
0.43
9(−
0.13
7)0.
174
(−0.
204)
0.23
5(−
0.16
9)0.
027∗
(0.3
16)
0.05
4(−
0.40
6)0.
825
(−0.
051)
0.01
7∗(−
0.41
3)0.
613
(0.0
80)
Zin
c0.
016
(0.4
09)
0.03
1∗(0
.319
)0.
001∗
(0.4
62)
0.92
6(0
.014
)0.
014∗
(0.5
06)
0.58
2(0
.127
)0.
000∗
(0.5
79)
0.89
1(−
0.02
2)Ir
on0.
935
(0.0
14)
0.56
4(0
.087
)0.
110
(0.2
27)
0.90
2(0
.018
)0.
582
(−0.
121)
0.77
7(−
0.06
6)0.
050∗
(−0.
344)
0.99
9(0
.000
)So
dium
0.65
4(−
0.08
0)0.
420
(0.1
22)
0.78
6(−
0.03
9)0.
791
(−0.
039)
0.26
0(0
.245
)0.
409
(0.1
9)0.
022∗
(0.3
97)
0.62
1(0
.079
)M
agne
sium
0.72
4(−
0.06
3)0.
878
(0.0
23)
0.81
8(0
.033
)0.
270
(0.1
61)
0.91
1(0
.025
)0.
167
(0.3
13)
0.13
5(−
0.26
6)0.
810
(0.0
38)
Pota
ssiu
m0.
758
(−0.
055)
0.03
8∗(−
0.30
7)0.
115
(−0.
224)
0.35
8(−
0.13
4)0.
009∗
(−0.
529)
0.61
2(−
0.11
7)0.
067
(−0.
322)
0.72
2(−
0.05
6)C
alci
um0.
813
(0.0
42)
0.53
7(0
.093
)0.
744
(0.0
47)
0.06
4(−
0.26
6)0.
400
(−0.
184)
0.55
2(−
0.13
7)0.
534
(0.1
12)
0.73
6(0
.054
)
Not
e.Sa
mpl
esi
ze=
#of
food
item
sin
each
grou
psdi
etth
atw
ere
cons
ider
ed,R
C=
red
colo
bus,
BW
C=
blac
k-an
d-w
hite
colo
bus,
LG=
larg
egr
oup
(K30
),SG=
smal
lgro
up(K
30),
Mik=
heav
ilylo
gged
fore
stat
Mik
ana,
Nk=
Cra
ter
Lak
eN
kuru
bafo
rest
frag
men
t.∗ p<
0.05
.
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Colobine Mineral Resources 557
Tabl
eV
.E
stim
ated
aver
age
min
eral
inta
ke(m
g/kg
)of
frug
ivor
ous/
omni
voro
uspr
imat
esin
Kib
ale
Nat
iona
lP
ark,
Uga
nda
(cal
cu-
late
dfr
omav
erag
em
iner
alco
nten
tof
food
item
cate
gori
es,
e.g.
,ri
pefr
uits
,un
ripe
frui
ts,
leav
es,
bark
,an
dpe
rcen
tage
inta
keof
food
item
cate
gori
esas
repo
rted
byW
rang
ham
etal
.(19
98))
Cu
Mn
Zn
FeN
aM
gK
Ca
Chi
mpa
nzee
(Pan
trog
lody
tes)
9.63
61.8
724
.08
154.
8716
2.93
1989
.77
1869
3.8
6641
.2B
lue
mon
keys
(Cer
copi
thec
usm
itis)
10.6
187
.86
25.7
514
2.26
168.
0420
59.4
116
158.
6662
52.5
Man
gabe
ys(L
opho
cebu
sal
bige
na)
10.3
83.2
824
.89
169.
6616
9.66
1976
.37
1559
2.9
6655
.3R
ed-t
aile
dm
onke
y(C
erco
pith
ecus
asca
nius
)10
.44
83.7
225
.03
170.
5217
0.52
2010
.92
1577
6.6
6272
.6
Not
e.Fo
odit
emm
iner
alco
nten
tsar
eba
sed
onav
erag
efr
omfo
ods
know
nto
beea
ten
by≥1
ofth
e4
spec
ies.
P1: FYJ
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558 Rode, Chapman, Chapman, and McDowell
Table VI. Results of a one-way ANOVA comparing mineral contents (mg/kg)of frugivorous/omnivorous primates to folivorous colobines in unlogged and lightly
logged areas of Kibale National Park, Uganda (n = 4 for all tests)
Cu Mn Zn Fe Na Mg K Ca
Mean – colobinesa 9.7 70.65 29.98 157.2 193.4 2608.33 17179.6 10251.5Mean – frugivores/ 10.25 79.2 24.94 143.9 167.8 2009.12 16555.5 6455.4
omnivoresF value 2.94 1.77 11.52 4.79 3.21 79.64 0.39 342.46p value 0.14 0.23 0.015 0.071 0.123 <0.001 0.554 <0.001
aValues for 2 groups of each colobus species, black and white colobus and red colobus.
These results are strikingly similar to those of Nagy and Milton (1979),Dierenfeld and McCann (1999), and Schwitzer and Kaumanns (2000). Al-though Dierenfeld and McCann (1999) did not describe total mineral intake,they also found Na content of naturally occurring foods to be exceedingly lowfor a semifree-ranging group of lion-tailed macaques (Macaca silenus) andring-tailed lemurs (Lemur catta) on St. Catherine’s Island, Georgia, U.S.A.Schwitzer and Kaumanns (2000) documented low intakes of Fe, Na, and Mnin 2 groups of captive black-and-white ruffed lemurs (Varecia variegata var-iegata) relative to suggested requirements. Na and Cu intake were also lowin wild-caught howlers that ate natural fruits and leaves (Nagy and Milton,1979; Table IV).
Evaluating whether Fe intake is insufficient is difficult because estimatesof intake values fall between the values suggested by Nicolosi and Hunt(1979) and the National Research Council (1978). Several researchers havesuggested that current estimates of Fe requirements for nonhuman primatesare too high (Dierenfeld and McCann, 1999; Dorrestein et al., 2000), whichis supported by evidence of hemosiderosis or Fe overload in some captiveprimates (Dorrestein et al., 2000; Spelman et al., 1989). Thus, it seems likelythat current recommended Fe requirements are above the true physiolog-ical needs of some primate groups. Further, primates are almost always atthe high end for mineral requirements in comparison to other mammaliantaxa (Robbins, 1993). Suggested requirements for Na, K, Mg, and Fe arehigher than for any other species, including humans (Oftedal, 1991; Robbins,1993). However, although the suggested Na requirement may also be high,intake levels fall far below listed requirements of most taxonomic groups.Thus, it is possible that they experience Na deficiency and Na resources arelimited.
Based on the low availability of Na to colobines, it is surprising thatonly one of the 8 groups selected foods that were high in Na. There are
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Colobine Mineral Resources 559
several possible explanations for this. First, Na content does not appear tobe highly variable among food items or species. This is evident from thelack of differences in Na content among young leaf species and food items.Na appears to be present at high concentrations only in plant parts of Eu-calyptus and at low concentrations in most other tree species. Without suf-ficient variation in Na concentration, correlations between selectivity andplant Na content are unlikely. Second, Na accumulation in plants is typi-cally associated with reduced concentrations of protein and other mineralsand high concentrations of secondary compounds (Masters et al., 2001).Protein is important in colobine dietary selection (Chapman and Chap-man, 2002), and it influences population size (along with fiber – Chap-man et al., 2002; Oates et al., 1990). Thus, overall, colobines may chooseto consume only the minimum amount necessary to meet their Na require-ments since overall, Na containing plants are low in other importantnutrients.
Although there is only one correlation between selectivity and Na con-tent, there is evidence that colobines and other primates in Kibale occasion-ally seek out resources high in Na. Oates (1978) found that black-and-whitecolobus in Kibale come to the ground and even wade through water to forageswamp plants with high Na concentrations. Other Na-limited herbivores useswamp plants as sources of Na (Fraser, 1979; Fraser et al., 1984; MacCrackenet al., 1993; Pletscher, 1987; Sun et al., 1997). Oates (1978) suggested that thepresence of swamp areas containing Na-rich plants partly explains the rela-tively high density of black-and-white colobus in the logged areas of Kibale(Oates, 1978). Kibale primates commonly drink from mud puddles (Chap-man and Rode, unpubl. data), which may be driven by the need to meet Narequirements. Most primates appear to meet their hydric needs from waterin foods (Nagy and Milton, 1979), suggesting that use of free water may bedriven by an alternative dietary requirement. Since mud-puddling behav-ior of tropical butterflies has been attributed primarily to Na consumption(Beck et al., 1999), consumption of water from mud puddles by primatescould serve the same purpose. Finally, urine consumption, a common symp-tom of Na deficiency, occurs in Kibale primates (Chapman unpubl. data,Lambert, 2000). Mountain goats, porcupines, and domestic cattle seek outurine soaked wood in response to Na deficiency (Blair-West et al., 1968, Mc-Dowell, 1992; Robbins, 1993). In addition, for 2 colobine groups, the dietaryselection analysis shows a negative correlation with K, which could be amechanism for Na conservation since lower K intake reduces Na excretion(Bell, 1995; Chiy and Phillips, 1995; Faber et al., 1993).
With the exception of Na and Fe, foods consumed by colobines in Kibaleare relatively well-balanced in terms of mineral nutrition. Although vari-ation in mineral content is high among young leaves of different species
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560 Rode, Chapman, Chapman, and McDowell
consumed by colobines, values are typically above suggested requirements.The presence of several key mineral resources appears to be important tomaintain high levels of mineral intake both seasonally and across groupsof both colobus species. All colobine groups obtained a majority of miner-als from major foods in their diet, such as Celtis durandii and C. africana.The high protein and low fiber content of Celtis durandii and C. africanacombined with their adequate mineral contents makes them important nu-tritional resources for Kibale Colobinae (Chapman and Chapman in press).Despite a majority of minerals being derived from these major foods, youngleaves of most tree species provide adequate mineral levels,which explains why mineral content among groups and seasons is relativelyconstant.
Seasonal variation in the dietary mineral content of colobines is muchless pronounced than seasonal variation in the leaves of individual trees(Baranga, 1983) in Kibale, which suggests that colobines may experiencepronounced seasonality in mineral availability, but buffer it with appro-priate food choices. The significance of seasonal variation is only impor-tant for minerals that drop below suggested requirements: Fe, Cu,and Na.
Frugivorous/omnivorous primates face more complex decisions rela-tive to maintaining adequate mineral intake since typical fruit-based dietsare lower in zinc, magnesium, calcium, and iron in comparison to colobusdiets dominated by leaves. However, estimates for frugivorous/omnivorousprimates in this study were still adequate in all minerals except iron andsodium. Because redtails and blue monkeys consume a relatively large pro-portion of their diet as invertebrates (>20%; Chapman et al., 2003), es-timates may change significantly when insects are included in mineral in-take calculations. Iron content of caterpillars is exceedingly high comparedto plant resources and compared to invertebrates analyzed from previ-ous studies (e.g., earthworms, mealworms, crickets, and fruit flies; Barkeret al., 1998), suggesting the importance of insects for frugivorousprimates.
Future research on primate mineral nutrition will be important for iden-tifying the significance of iron and sodium deficiencies in primate diets. Be-cause sodium appears to be limiting, artificial resources of sodium, such assodium blocks, may be useful in managing primate habitat use, particularlyrelative to crop raiding activities. Sodium resources have been an effec-tive management tool for controlling movement patterns in some species(Conover, 1998; Hailey and Coulson, 1996) and are known to effect wildlifehabitat use (Faber et al., 1993; Hailey and Coulson, 1996; Mattfield et al.,1972; Miller and Litvaitis, 1992).
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Colobine Mineral Resources 561
AP
PE
ND
IXA
.M
iner
alco
mpo
siti
on(m
g/kg
)of
plan
tsam
ples
from
Kib
ale
Nat
iona
lPar
k,U
gand
a.
N%
Ash
Cu
Mn
Zn
FeN
aM
gK
Ca
Bar
ksA
lang
ium
chin
ense
116
.05
3.16
46.1
53.
1846
.42
28.1
244
0.31
9416
.25
3511
8.62
Alb
izia
gran
dibr
acte
ata
17.
813.
8229
.44
7.13
81.8
71.8
938
4.93
2575
.63
2015
2.16
Dom
beya
muk
ole
110
.94
5.47
19.5
85.
9335
.08
187.
6312
18.2
485
38.5
519
687.
61E
ucal
yptu
ssp
.3
11.9
97.
2520
5.64
23.4
316
7.50
949.
9528
08.6
064
84.8
728
547.
31P
runu
saf
rica
na1
6.50
6.69
91.3
823
.81
131.
5016
7.05
2348
.24
3035
1.30
1640
4.73
Cro
psSw
eetp
otat
otu
bers
12.
433.
7918
.53
5.67
35.0
314
4.85
676.
992
17.9
1324
.7Ir
ish
pota
totu
bers
13.
524.
596.
9016
.23
38.9
687
.21
807.
614
243.
343
.9B
anan
api
th1
10.4
02.
0793
.48
24.7
284
.21
163.
8714
03.5
4551
8.9
2030
.7B
anan
ale
aves
19.
057.
0830
3.74
14.5
092
.03
141.
6720
84.9
2935
4.3
2852
.3M
aize
cob
11.
713.
3411
.00
25.6
967
.67
8.23
666.
427
27.2
Mai
zele
aves
111
.58
7.15
40.7
913
.93
116.
7840
.10
1758
.513
276.
534
49.2
Cas
sava
tube
r1
1.97
1.15
5.68
7.33
41.2
011
9.66
978.
861
40.3
957.
8F
low
ers
Cel
tisdu
rand
ii1
8.67
14.7
363
.54
57.9
919
2.47
171.
1528
55.2
625
312.
3980
50.6
7C
ordi
aab
yssi
nica
19.
329.
3821
.78
27.2
219
4.59
158.
6818
97.5
920
626.
7851
13.2
0E
ryth
rina
abys
sini
ca2
9.24
13.9
695
.91
47.2
713
4.38
125.
7731
54.3
621
713.
3068
67.4
9Ja
cara
nda
mim
osif
olia
43.
3114
.36
51.6
131
.94
161.
7315
5.76
1775
.10
1511
0.70
6381
.00
Mar
kham
iapl
atyc
alyx
12.
4719
.06
48.6
482
.69
214.
4693
.74
1335
.39
1675
8.64
2414
.31
Mon
odor
am
yris
tica
110
.56
33.8
430
.93
36.6
512
3.46
88.0
739
84.3
117
274.
146
71.0
8Sy
mph
onia
glob
ulif
era
13.
477.
5110
4.53
21.1
877
.70
78.6
922
14.7
811
311.
4788
88.2
4Tr
agia
sp.
113
.99
18.0
157
.67
48.6
263.
9713
1.07
3795
.66
1588
5.17
1341
5.89
Rip
eFr
uit
Alb
izia
gran
dibr
acte
ata
24.
433.
5325
.01
25.5
910
0.11
146.
6779
7.94
1337
5.17
3719
.21
Ani
nger
iaal
tissi
ma
14.
396.
328.
8314
.37
130.
2214
8.98
430.
3912
387.
4427
42.3
4
P1: FYJ
International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
562 Rode, Chapman, Chapman, and McDowellA
PP
EN
DIX
A.
(Con
tinu
ed.)
N%
Ash
Cu
Mn
Zn
FeN
aM
gK
Ca
Bri
delia
mic
rant
ha2
4.41
7.23
47.8
525
.63
133.
1535
9.11
2433
.63
1193
6.79
1032
7.32
Cel
tisdu
rand
ii1
7.87
16.4
146
.89
25.4
632
9.35
115.
8521
18.4
669
23.6
1335
0.69
Cha
etac
me
aris
tata
18.
458.
9020
.99
17.2
516
2.04
78.9
297
3.94
9613
.45
906.
77C
ordi
am
illen
ii1
7.65
11.5
67.
239.
2241
.99
139.
298
1.84
3094
0.75
645.
94C
ordi
aab
yssi
nica
18.
874.
4756
.646
.31
1235
.74
184.
0988
3.43
2081
6.14
5660
.3D
asyl
epis
egge
lingi
i1
7.18
6.56
51.5
97.
8818
2.24
183.
3618
61.6
122
457.
1037
06.4
0D
iosp
yros
abys
sini
ca2
4.69
423
.112
.24
56.4
658
.48
725.
9215
901.
1829
38.2
6D
ovya
lissp
.1
5.55
6.57
10.9
111
.75
100.
917
9.99
1058
.12
1960
7.95
1554
.46
Ehr
etia
cym
osa
18
6.44
25.8
824
.22
167.
0896
.19
1935
.15
2101
127
50.8
4E
uade
nia
emin
ens
18.
985.
0124
.43
17.6
197
.54
207.
9924
75.6
3026
3.82
2304
.45
Euc
alyp
tus
sp.
14.
675.
0031
7.69
10.8
996
.24
967.
9623
18.2
111
032.
7710
386.
76F
icus
brac
hyle
pis
25.
419.
176.
1311
.51
67.6
473
.48
1978
.95
1421
8.72
5104
.932
Fic
usca
pens
is3
8.40
14.4
434
.79
64.1
319
5.65
115.
8926
50.2
926
568.
6941
53.8
2F
icus
exas
pera
ta2
10.8
18.
1726
.53
13.8
810
7.49
132.
3422
64.8
721
898.
7190
47.3
7F
icus
nata
lens
is1
5.69
7.61
37.0
614
.52
65.2
717
6.99
1438
.05
1396
5.71
6012
.17
Fic
usst
ipul
ifer
a1
9.51
11.0
49.
349.
2487
.73
200.
6428
41.2
332
770.
3788
29.3
2F
icus
urce
olar
is1
11.1
7.86
40.2
717
.05
203.
4821
7.19
3588
.421
993.
4210
174.
24F
untu
mia
lati
foli
a3
6.93
10.2
015
.08
37.3
566
.44
141.
9314
70.8
415
702.
4176
3.95
Kig
elia
moo
sa1
3.43
6.35
6.02
2.89
47.5
316
3.94
529.
4112
874.
1936
0.96
Lin
dack
eria
sp.
18.
0110
.34
89.4
21.4
211
6.82
122.
3119
14.1
719
114.
3242
78.1
Lin
ocie
rajo
hnso
nii
14.
2111
.92
13.0
515
.98
75.4
814
3.01
822.
8913
081.
1332
23.4
6L
ychn
odis
cus
cero
sper
mus
15.
7410
.66
151.
9913
.79
225.
2486
.46
1723
.68
1269
3.57
5363
.79
Mae
sala
nceo
lata
18.
658.
7967
.11
21.2
489.
0135
8.22
1721
.85
2611
5.82
7541
.84
Mar
kham
iapl
atyc
alyx
15.
0411
.32
35.7
814
.22
90.4
710
9.12
874.
0215
538.
1143
95.6
5M
illet
tiadu
ra1
2.42
8.05
23.8
112
.32
49.8
210
9.87
1255
.37
1168
1.73
4720
.78
Mim
usop
sba
gsha
wei
23.
971.
6529
.02
3.82
255.
0812
1.12
759.
1191
81.9
429
35.9
9M
onod
ora
myr
istic
a1
5.35
10.7
28.
6413
.78
75.9
61.5
811
34.4
259
42.2
219
93.3
4M
yria
nthu
sho
lstii
19.
5826
.54
93.4
522
.96
165.
7897
.66
3255
.42
3228
0.66
3392
.2N
eobo
uton
iam
acro
caly
x4
8.51
13.0
848
.17
37.2
321
2.60
183.
6132
31.5
927
605.
0111
256.
43O
lea
wel
wits
chii
16.
828.
4619
.72
18.4
323
9.91
233.
3314
56.9
614
323.
1281
77.6
Pip
ergu
inen
sis
19.
9915
.45
20.7
510
.414
9.16
223.
7324
39.2
232
270.
5519
68.1
9P
sidi
umgu
ajav
a1
4.41
6.24
19.8
510
.84
201.
218
4.43
747.
6315
887.
1512
64.3
8P
runu
saf
rica
na3
4.31
7.88
13.6
819
.23
122.
0585
.69
1821
.72
1202
4.77
2786
.58
P1: FYJ
International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
Colobine Mineral Resources 563R
othm
anni
aur
celli
form
is2
5.45
16.0
422
.36
11.6
969
.76
178.
3213
17.0
215
191.
4212
38.7
9Sp
atho
dea
cam
panu
lata
26.
8010
.56
28.0
023
.68
51.6
312
5.95
2169
.94
2224
4.72
6950
.19
Stry
chno
sm
itis
16.
431.
475.
534.
1213
.83
51.4
728
2.23
1153
8.21
807.
95Ta
bern
aem
onta
nasp
.1
6.51
16.4
314
0.51
30.4
815
9.74
71.5
920
08.7
620
915.
719
98.0
8T
rem
aor
ient
alis
114
.93
9.52
228.
1851
.95
310.
475
53.8
1530
55.1
210
182.
1392
11.5
4U
vari
opsi
sco
ngen
sis
78.
9314
.29
20.0
319
.65
79.7
871
.15
1781
.95
3296
5.52
3263
.11
Van
guer
iaap
icul
ata
17.
477.
5684
.62
9.83
97.8
712
5.65
564.
1413
932.
5810
51.3
5
Unr
ipe
frui
tB
ride
liasp
.1
4.21
16.8
125
.92
38.5
424
7.33
132.
0814
76.1
1673
3.5
5493
.2C
elti
sdu
rand
ii3
10.5
110
.11
55.1
223
.76
139.
8890
.24
3566
.111
455.
112
249.
9E
ucal
yptu
ssp
.1
4.77
5.79
17.4
914
.07
109.
5253
7.87
1768
.872
84.7
6279
.3F
icus
nata
lens
is4
6.16
11.4
830
.32
22.6
781
.40
184.
0216
64.7
2244
3.7
5117
.5St
rych
nos
miti
shu
sks
34.
2311
.17
65.5
017
.03
34.6
714
9.15
770.
511
750.
716
67.7
Mix
edle
aves
Aca
lyph
asp
.lea
ves,
twig
s1
12.0
721
.75
23.0
845
.15
64.0
511
8.87
1863
.921
899.
025
62.1
Ala
ngiu
mch
inen
se1
8.59
4.31
33.3
510
.76
88.5
411
5.22
2207
.460
94.6
9211
.6A
lbiz
iagr
andi
brac
teat
a1
5.02
10.2
264
.77
19.8
292
.11
160.
4526
08.8
2100
6.7
1125
5.1
Ant
iari
sto
xica
ria
111
.47
11.9
694
5.28
24.7
433
.44
27.7
734
73.4
1538
6.3
9486
.8B
ligh
iaun
ijug
ata
16.
357.
6426
.26
20.3
451
.36
161.
6544
00.2
1088
3.8
9500
.7B
osqu
eia
phob
eros
110
.19
17.9
529
.06
45.2
766
.67
7.98
1589
.987
47.0
1407
.5D
iosp
yros
abys
sini
ca1
7.04
8.65
363.
6426
.86
421.
1579
.96
2218
.011
856.
812
776.
8D
raca
ena
sp.
19.
6516
.54
16.8
024
.90
49.7
412
1.45
3856
.890
12.1
4147
.5E
ryth
roph
leum
sp.
110
.96
14.8
590
4.66
26.0
822
9.57
191.
8278
40.0
1884
1.9
1424
4.3
Fic
usas
peri
folia
leaf
/tw
ig1
12.0
09.
7051
.72
27.1
115
5.74
114.
4848
58.1
1205
8.1
1591
6.7
Lee
agu
inen
sis
19.
1112
.91
1.74
16.2
611
6.91
107.
0220
59.0
1718
7.4
3774
.8M
imus
ops
bags
haw
ei1
6.48
6.90
8.56
21.5
414
6.05
164.
3014
77.6
2564
3.5
1437
.6N
ewto
nia
bucc
hana
ni1
3.90
11.9
788
.39
24.1
799
.71
113.
1915
20.0
6710
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18.5
Phy
tola
cca
sp.
119
.36
6.80
588.
6837
.76
269.
1712
3.20
1082
8.2
4081
6.8
3213
9.2
Rot
hman
nia
urce
llif
orm
is1
6.16
12.1
063
.16
22.4
653
8.96
157.
6234
59.3
1419
7.2
6115
.7T
rich
ilia
sple
ndid
a1
8.31
7.83
22.0
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.14
163.
1412
4.56
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.513
916.
543
04.5
Uva
riop
sis
cong
ensi
s1
10.3
26.
3923
4.37
10.5
388
.68
55.9
525
76.0
1332
8.5
1286
9.2
P1: FYJ
International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
564 Rode, Chapman, Chapman, and McDowell
AP
PE
ND
IXA
.(C
onti
nued
.)
N%
Ash
Cu
Mn
Zn
FeN
aM
gK
Ca
Mat
ure
leav
esA
cant
hus
pube
scen
s2
8.70
7.77
73.8
134
.69
132.
1011
1.17
5544
.912
530.
411
277.
4A
lbiz
iagr
andi
brac
teat
a2
5.09
5.10
46.2
615
.12
92.2
819
4.40
1674
.915
751.
072
44.2
Bos
quei
aph
ober
os1
8.51
7.70
142.
368.
2374
.24
75.3
524
27.3
1445
8.3
4526
.6C
assi
pour
earu
wen
sore
nsis
18.
233.
5815
9.09
9.48
93.4
011
5.57
2979
.425
720.
113
109.
5C
elti
saf
rica
na2
17.9
65.
6832
.53
13.2
468
.77
76.7
617
20.6
3252
8.3
5644
.0C
elti
sdu
rand
ii3
12.3
79.
5087
.80
24.1
215
2.49
213.
9724
32.1
1736
6.2
5875
.5C
haet
acm
ear
ista
ta1
14.9
410
.39
76.7
57.
1341
.94
100.
5922
55.8
1178
6.3
5482
.0C
laus
ena
anis
ata
112
.38
10.4
336
.43
55.4
812
7.27
120.
5019
61.8
1946
9.5
1516
.4D
iosp
yros
abys
sini
ca1
9.49
8.32
57.2
812
.47
63.9
858
.09
1555
.213
866.
024
30.6
Dom
beya
muk
ole
311
.45
4.92
52.1
618
.23
116.
5211
0.81
2720
.613
711.
379
87.5
Fic
usex
aspe
rata
116
.53
4.75
114.
7211
.04
59.8
288
.04
1438
.716
809.
814
90.8
Fic
usna
tale
nsis
210
.91
5.99
36.4
625
.37
158.
4431
5.25
2226
.723
374.
116
788.
3F
untu
mia
lati
foli
a2
6.64
7.69
253.
0121
.13
565.
6017
81.9
932
71.1
1625
8.6
8234
.1Il
exm
itis
114
.50
4.96
313.
7812
.36
77.2
310
8.66
2322
.213
927.
713
944.
0L
epto
nych
iam
ildbr
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i1
11.0
911
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33.6
437
.92
90.8
815
3.27
5965
.319
151.
911
670.
2M
arkh
amia
plat
ycal
yxle
aflet
s3
5.76
16.5
431
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15.7
570
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178.
5824
05.8
9491
.311
960.
2M
arkh
amia
plat
ycal
yx2
7.70
12.0
743
.22
18.5
218
0.93
106.
7331
04.2
9278
.918
147.
9le
aflet
san
dpe
tiol
esM
ille
ttia
dura
25.
929.
0010
3.20
15.3
314
3.99
101.
8718
52.2
1663
9.0
5074
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imus
ops
bags
haw
ei2
7.85
2.59
60.0
68.
6416
1.97
76.0
437
14.6
4672
.915
798.
9N
eobo
uton
iam
acro
caly
x1
10.9
39.
5631
6.41
25.4
115
8.48
129.
8246
99.4
2138
8.3
1589
7.9
Ole
aw
elw
itsch
ii1
5.73
5.36
236.
108.
5782
.20
123.
7119
59.4
1487
7.4
1039
2.6
Pan
covi
atu
rbin
ata
16.
864.
5424
4.84
8.71
34.5
570
.46
2908
.210
011.
331
666.
2P
arin
ari
exce
lsa
15.
614.
6333
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4.07
64.0
282
.77
3741
.910
017.
814
383.
8P
runu
saf
rica
na4
7.38
5.34
18.7
311
.16
99.8
116
3.18
2836
.011
757.
011
265.
2St
rom
bosi
asc
heffl
eri
210
.05
6.58
371.
7412
.88
594.
3814
4.15
3677
.310
339.
715
798.
4St
rych
nos
miti
s1
11.8
45.
9616
3.48
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94.8
387
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3363
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949.
310
503.
3Te
clea
nobi
lis
113
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9.96
41.0
725
.81
76.8
748
.01
2744
.730
305.
110
035.
1U
vari
opsi
sco
ngen
sis
111
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6.46
91.6
110
.36
90.2
596
.79
5684
.720
066.
712
105.
5V
erno
nia
sp.
211
.60
6.67
103.
9228
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263.
7312
6.14
2872
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104.
611
802.
3
P1: FYJ
International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
Colobine Mineral Resources 565
Lea
fbud
sC
elti
sdu
rand
iile
afbu
ds1
9.38
25.5
982
.57
80.4
343
2.48
426.
2530
36.9
2509
3.1
8687
.0F
icus
daw
eite
rmin
alL
111
.46
6.51
17.7
511
.80
71.0
925
6.55
4551
.312
066.
928
593.
3P
etio
les
Alb
izia
gran
dibr
acte
ata
211
.87
7.60
36.0
533
.00
109.
2613
7.13
2204
.44
1980
7.84
1444
8.90
Bri
delia
mic
rant
ha1
17.9
35.
8463
3.99
103.
5111
4.46
241.
4650
00.6
680
81.5
437
801.
82C
arap
agr
andi
flora
114
.14
5.68
138.
0138
.78
117.
9224
1.08
2102
.16
1755
6.83
2014
8.14
Dom
beya
muk
ole
116
.60
6.76
36.1
629
.79
203.
0311
4.08
5252
.71
2287
0.80
3509
0.19
Faga
rops
isan
gole
nsis
49.
689.
6861
.53
33.0
719
0.85
135.
3836
89.0
418
176.
6810
293.
68M
arkh
amia
plat
ycal
yx4
14.0
311
.86
47.7
043
.60
310.
9613
8.30
3933
.55
3020
5.52
2168
4.15
Myr
iant
hus
hols
tii1
7.59
14.7
888
.73
31.0
520
3.05
133.
7743
06.7
1358
2.13
9343
.69
Ole
aw
elw
itsch
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8.83
4.75
18.7
934
.51
167.
3410
5.39
3102
.27
1395
6.67
1321
3.74
Stro
mbo
sia
sche
ffler
i4
13.4
99.
1072
.65
49.7
611
1.62
178.
2042
65.7
629
765.
6325
908.
75Se
eds
Bal
anite
sw
ilson
iana
husk
s1
5.74
6.2
26.5
93.
4211
.32
83.1
855
4.51
1773
8.72
831.
77B
alan
ites
wils
onia
nain
side
s1
4.81
12.6
725
.62
17.2
710
2.49
39.0
212
46.2
116
276.
511
12.2
8C
elti
sdu
rand
ii1
8.69
12.4
710
8.93
28.5
931
3.73
2.18
1633
.99
3758
.17
1111
.11
Chr
ysop
hyllu
msp
.1
2.9
5.62
61.2
614
.36
21.3
245
.65
1087
.14
3964
.15
2594
.72
Das
ylep
iseg
gelin
gii
22.
8314
.36
81.1
628
.14
70.4
824
4.54
1366
.85
5179
.08
2701
.66
Fun
tum
iala
tifol
ia(p
od)
14.
3114
.612
6.55
23.9
37.5
623
.727
02.4
388
23.2
344
77.1
6M
aesa
lanc
eola
ta1
7.78
6.55
60.8
819
.42
136.
3123
2.2
1847
.94
1796
7.59
6518
.98
Mar
anta
cloa
sp.
17.
995.
1269
.92
13.9
329
8.99
153.
8365
4.48
1088
0.02
285.
29M
arkh
amia
plat
ycal
yx(s
eeds
from
pods
)1
5.26
8.27
29.8
723
.87
122.
2525
5.57
652.
7615
129.
5639
88.4
5O
xyan
thus
sp.
13.
0315
.96
53.1
138
.45
197.
4332
.45
1986
.59
7425
.11
2094
.77
Pitt
ospo
rum
sp.
13.
068.
5380
.76
23.2
452
.95
328.
9314
81.5
156
96.0
426
84.8
9P
seud
ospo
ndiu
sm
icro
carp
a2
4.27
7.39
15.5
79.
6566
.97
62.4
410
19.6
213
876.
4910
85.9
9P
runu
sA
fric
ana
12.
9510
.81
13.0
466
.87
267.
4289
.94
1359
.484
44.7
932
68.0
6U
nkno
wn
shru
b1
3.55
4.93
8.89
14.7
461
.87
49.6
412
52.1
513
447.
6353
27.1
9U
rella
sp.
19.
1912
.35
57.8
531
.317
7.17
279.
9626
75.6
215
547.
5216
177.
69
P1: FYJ
International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
566 Rode, Chapman, Chapman, and McDowellA
PP
EN
DIX
A.
(Con
tinu
ed.)
N%
Ash
Cu
Mn
Zn
FeN
aM
gK
Ca
You
ngle
aves
Aca
cia
vine
27.
035.
1839
.79
46.1
211
6.04
141.
7913
67.8
1038
3.7
1528
0.0
Aca
lyph
asp
.1
9.21
11.0
148
.26
28.1
717
7.59
138.
2843
57.1
2505
2.6
9497
.8A
cant
hus
pube
scen
s1
8.60
15.8
449
.94
42.0
310
4.02
153.
4050
95.6
1739
8.9
8995
.1A
lbiz
iagr
andi
brac
teat
a11
6.44
11.9
951
.98
41.6
414
0.51
170.
4625
62.8
2012
6.0
5915
.0B
ligh
iaun
ijug
ata
126.
598.
9729
.24
27.4
011
9.96
138.
2129
54.0
1528
2.8
3632
.5B
osqu
eia
phob
eros
57.
919.
1891
.15
20.7
013
3.09
132.
7726
99.7
1689
6.1
1003
4.7
Cas
sipo
urea
ruw
enso
rens
is1
8.11
7.19
1634
.11
5.56
55.3
675
.15
1773
.296
28.1
7140
.9C
elti
saf
rica
na21
12.8
37.
6371
.33
31.8
313
3.94
122.
9330
67.7
1361
5.2
2288
7.5
Cel
tis
dura
ndii
278.
819.
5264
.05
35.1
420
7.54
146.
9421
76.1
1812
1.1
7165
.7C
haet
acm
ear
ista
ta2
9.55
5.67
69.6
65.
5320
.73
95.9
330
10.5
1067
0.8
8232
.5C
laus
ena
anis
ata
17.
6113
.68
26.0
744
.75
85.5
917
1.18
2675
.025
703.
549
93.1
Cor
dia
abys
sini
ca1
10.7
312
.06
34.0
513
.60
70.8
835
.44
1984
.910
851.
923
79.2
Dio
spry
osab
yssi
nica
75.
596.
3513
5.01
25.6
510
6.41
66.0
422
31.5
1477
7.9
7673
.3D
ombe
yam
ukol
e14
9.65
10.2
365
.48
36.2
615
1.05
448.
4433
99.9
2272
7.4
1199
9.1
Ehr
etia
cym
osa
19.
144.
1658
.33
32.8
994
.84
56.5
217
65.9
1844
4.8
6688
.7E
ryth
rina
abys
sini
ca1
7.06
19.4
960
.29
58.9
315
2.41
224.
9220
79.2
2512
9.2
2953
.3E
ryth
rina
abys
sini
ca(n
ope
tiol
e)1
7.80
18.3
211
8.66
38.5
919
2.95
37.2
826
69.8
2026
6.3
3383
.8E
ucal
yptu
ssp
.4
5.39
7.22
237.
2024
.39
106.
3216
46.8
129
86.4
1181
4.8
5531
.0F
icus
aspe
rifo
lia1
11.8
18.
4262
.68
32.0
612
1.18
128.
9037
31.2
2151
9.1
1471
9.8
Fic
usca
pens
is1
8.15
9.53
11.5
220
.31
281.
7777
.53
1090
.781
42.0
1422
.8F
icus
exas
pera
ta5
14.1
99.
0946
.03
22.8
314
4.20
111.
1325
61.4
1652
4.0
7300
.7F
icus
nata
lens
is4
15.3
87.
3436
.00
24.1
412
2.08
190.
5922
54.2
2304
7.9
1560
5.8
Fic
usva
llis
210
.30
3.12
32.0
529
.17
175.
3912
9.27
6339
.010
223.
914
495.
0F
untu
mia
lati
foli
a2
5.30
10.7
570
.26
22.8
415
8.39
133.
8726
65.5
1536
4.3
4254
.3Il
exm
itis
112
.00
16.5
514
3.91
28.7
892
.47
249.
8741
23.3
9443
.932
547.
8L
epto
nych
iam
ildb
raed
ii1
9.70
14.0
110
2.03
50.2
671
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169.
2431
28.4
1835
4.6
5328
.2M
acar
anga
sp.
15.
499.
3615
2.91
22.4
98.
9812
9.51
2184
.911
808.
641
60.2
Mae
sala
nceo
lata
48.
449.
2937
.45
30.9
215
4.05
172.
7117
10.1
1619
9.6
6552
.5M
arkh
amia
plat
ycal
yx6
7.37
17.1
129
.40
38.3
210
9.06
218.
5319
40.7
2512
4.3
4408
.0M
ille
ttia
dura
75.
8110
.32
103.
2129
.48
144.
8414
5.95
1936
.514
383.
828
96.2
Mim
usop
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44.
545.
6231
.11
22.0
311
5.80
141.
6820
16.7
1116
7.2
6914
.9N
eobo
uton
iam
acro
caly
x1
10.3
021
.01
165.
2133
.11
105.
5185
.51
3488
.112
132.
514
978.
5
P1: FYJ
International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
Colobine Mineral Resources 567
Ole
aw
elw
itsc
hii
88.
346.
1824
.82
16.8
372
.97
122.
6312
08.5
1218
1.1
5447
.0P
anco
via
turb
inat
a2
5.88
5.87
43.1
39.
4528
.12
100.
7414
55.1
6988
.746
13.7
Par
inar
iex
cels
a5
4.40
10.2
738
.65
21.9
111
0.83
113.
9631
42.8
1158
0.5
1073
5.4
Pol
ysci
asfu
lva(
nope
tiol
e)1
5.02
13.9
210
0.85
37.9
622
7.71
75.2
723
42.1
1272
5.8
4578
.6P
olys
cias
fulv
a3
5.59
8.67
36.5
333
.01
128.
7718
3.28
3001
.321
720.
049
81.9
Pru
nus
afri
cana
145.
088.
0161
.84
33.5
226
9.66
132.
3627
04.2
1495
4.9
7355
.3R
othm
anni
aur
cell
ifor
mis
16.
0310
.10
61.8
317
.69
120.
9073
.42
2031
.537
26.3
2798
.9Sp
atho
dea
cam
panu
lata
16.
5510
.74
18.8
523
.92
115.
8981
.18
2362
.917
629.
558
98.4
Stro
mbo
sia
sche
ffler
i4
6.93
11.9
571
.97
23.3
210
6.39
221.
8030
93.2
2215
1.6
7044
.0St
rych
nos
mit
is4
7.91
6.51
30.9
918
.48
107.
9011
1.66
2595
.218
407.
475
84.2
Tecl
eano
bili
s4
7.41
12.1
096
2.33
37.1
779
.32
126.
2026
70.3
2074
5.1
1338
2.0
Uva
riop
sis
cong
ensi
s1
7.94
11.5
652
.46
13.0
824
.01
107.
5119
39.6
2645
1.9
9184
.3V
erno
nia
sp.
111
.07
2.77
41.7
916
.87
277.
6412
0.80
3337
.379
36.4
2512
7.5
Not
e.B
old
spec
ies
are
cons
umed
byco
lobi
nes.
Min
eral
valu
esin
bold
are
belo
wre
quir
emen
tsfo
rno
nhum
anpr
imat
es(N
atio
nal
Res
earc
hC
ounc
il19
78).
P1: FYJ
International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
568 Rode, Chapman, Chapman, and McDowell
AP
PE
ND
IXB
.M
iner
also
urce
sof
colo
bine
sin
Kib
ale
Nat
iona
lP
ark,
Uga
nda
(per
cent
ages
repr
esen
tth
e%
ofto
talm
iner
alco
nten
ttha
tis
cont
ribu
ted
byea
chfo
odit
em
Bla
ck-a
nd-w
hite
colo
bus
(Col
obus
guer
eza)
Red
colo
bus
(Pili
ocol
obus
badi
us)
K30
Lar
geG
K30
Smal
lGM
ikan
aN
kuru
baK
30L
arge
GK
30Sm
allG
Mik
ana
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ruba
Food
%Fo
od%
Food
%Fo
od%
Food
%Fo
od%
Food
%Fo
od%
Cop
per
C.d
.YL
32.8
C.d
.YL
29.3
C.d
.YL
24.3
Alb
.YL
41.5
C.d
.YL
20.0
Par
.YL
11.0
C.d
.YL
15.4
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.YL
18.3
Mar
k.Y
L18
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L9.
9A
lb.Y
L12
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omb.
YL
8.3
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m.Y
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5C
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L11
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L14
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L10
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YL
9.6
Cd
UR
F12
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YL
8.0
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.YL
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14.4
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ines
ML
4.0
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.YL
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YL
8.8
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International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
Colobine Mineral Resources 569
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International Journal of Primatology [ijop] PP811-ijop-463017 May 8, 2003 12:51 Style file version Nov. 18th, 2002
570 Rode, Chapman, Chapman, and McDowell
ACKNOWLEDGMENTS
Funding for this research was provided by Wildlife Conservation So-ciety, the National Science Foundation (grant number SBR-9617664, SBR-990899), and the Leakey Foundation. Permission to conduct research wasgiven by the Office of the President, Uganda, National Council for Scienceand Technology, Uganda Wildlife Authority, and Ugandan Forest Depart-ment. We would like to thank Matt Burgess, Ashley Seifert, MikeWasserman, and Nancy Wilkinson for help with mineral analyses and thetwo anonymous reviewers for their helpful comments.
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