Mineral Resource Availability and Consumption by Colobus in...

P1: FYJ

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

P1: FYJ


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.

P1: FYJ


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

P1: FYJ



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.

P1: FYJ



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.

P1: FYJ



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

P1: FYJ



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

P1: FYJ



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

P1: FYJ



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.

P1: FYJ



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.

P1: FYJ



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).

P1: FYJ



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

P1: FYJ



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



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.

P1: FYJ



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



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

.

P1: FYJ



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



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

P1: FYJ



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

P1: FYJ



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).

P1: FYJ



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


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


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

.439

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

528

.14

163.

1412

4.56

2386

.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



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

aedi

i1

11.0

911

.69

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

.82

15.7

570

.50

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

.7M

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

.21

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

6.89

94.8

387

.35

3363

.124

949.

310

503.

3Te

clea

nobi

lis

113

.88

9.96

41.0

725

.81

76.8

748

.01

2744

.730

305.

110

035.

1U

vari

opsi

sco

ngen

sis

111

.71

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

.85

263.

7312

6.14

2872

.913

104.

611

802.

3

P1: FYJ



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

ii2

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


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

.53

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

sba

gsha

wei

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



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



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

Nku

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

Alb

.YL

18.3

Mar

k.Y

L18

.0C

.a.Y

L9.

9A

lb.Y

L12

.8C

.a.Y

L8.

9D

omb.

YL

8.3

Stro

m.Y

L7.

5C

.a.Y

L11

.1P

ru.Y

L14

.6C

.a.Y

L10

.6M

ark.

YL

9.6

Cd

UR

F12

.7P

ru.Y

L8.

6M

ark.

YL

8.0

C.a

.YL

7.4

Mar

k.Y

L10

.1D

omb.

YL

14.4

Dom

b.Y

L7.

8P

ru.Y

L6.

3C

.d.L

B12

.5V

ines

ML

4.0

Bos

.YL

7.8

C.d

.YL

7.0

Mil.

YL

8.8

C.a

.YL

8.2

C.d

.YL

5.5

Alb

.YL

5.5

C.a

.YL

8.2

Stry

c.Y

L3.

6P

ar.Y

L7.

6F

unt.

YL

6.8

Ole

aY

L8.

3B

lig.Y

L5.

1M

anga

nese

C.d

.YL

35.0

C.d

.YL

24.7

C.d

.YL

30.0

Tec.

YL

25.9

C.d

.YL

18.4

Euc

.Bar

k12

.7C

.a.Y

L14

.9E

uc.Y

L17

.5C

.a.Y

L15

.8C

.a.Y

L11

.6C

.a.Y

L13

.9A

lb.Y

L16

.6Te

c.Y

L12

.0C

.a.Y

L9.

0C

.d.Y

L14

.9P

ru.Y

L14

.6D

omb.

YL

7.9

Euc

.Bar

k11

.4C

.d.U

RF

12.6

Phy

t.M

L14

.1B

os.Y

L10

.6B

os.Y

L6.

3M

il.Y

L12

.6D

omb.

YL

11.9

Tec.

YL

5.6

Euc

.YL

7.5

Alb

.YL

10.1

C.a

.YL

7.7

C.a

.YL

7.6

C.d

.YL

6.2

Dio

s.Y

L7.

4A

lb.Y

L10

.3M

ark.

YL

4.9

Euc

.RF

6.5

Mil.

YL

7.9

Euc

.YL

6.4

Dom

b.Y

L7.

3St

rom

.YL

5.9

Dom

bY

L5.

3C

.a.Y

L10

.0Z

inc

C.d

.YL

36.6

C.d

.YL

34.3

C.d

.YL

25.7

Alb

.YL

36.8

C.d

.YL

24.2

C.a

.YL

10.8

C.d

.YL

18.1

Alb

.YL

17.6

C.a

.YL

13.4

C.a

.YL

13.1

Alb

.YL

12.8

C.a

.YL

9.5

Dom

b.Y

L9.

7C

.d.Y

L9.

0C

.a.Y

L14

.8P

ru.Y

L17

.0M

ark.

YL

12.2

Pru

.YL

8.3

C.d

.LB

11.3

Vin

esM

L9.

1C

.a.Y

L8.

2P

ar.Y

L8.

1M

il.Y

L8.

0D

omb.

YL

14.1

Dom

b.Y

L8.

4M

ark.

YL

6.8

C.a

.YL

9.8

Pru

.YL

9.1

Mar

k.P

et7.

6P

ru.Y

L7.

3M

ark.

YL

7.2

C.a

.YL

9.5

Alb

.YL

4.8

Alb

.YL

6.4

C.d

.UR

F8.

6C

laus

.YL

3.0

Mar

k.Y

L5.

9A

lb.Y

L5.

9O

lea

YL

7.2

Vin

esY

L5.

7Ir

onC

.d.Y

L44

.8C

.d.Y

L36

.7C

.d.Y

L32

.2A

lb.Y

L30

.7C

.d.Y

L27

.2P

ru.Y

L10

.7C

.d.Y

L22

.4P

ru.Y

L26

.5C

.a.Y

L11

.7P

ru.Y

L12

.1C

.d.L

B12

.9P

ru.Y

L18

.1M

ark.

Pet

10.3

C.d

.YL

9.8

C.a

.YL

13.0

Alb

.YL

11.6

Dom

b.Y

L7.

2C

.a.Y

L10

.0C

.d.U

RF

10.7

C.a

.YL

9.8

Dom

b.Y

L7.

7C

.a.Y

L8.

3M

il.Y

L8.

2D

omb.

YL

11.5

Mar

k.Y

L7.

2C

hry.

YL

5.1

Alb

.YL

9.2

Vin

esM

L5.

7B

os.Y

L7.

1P

ar.Y

L7.

6O

lea

YL

6.5

Mim

.ML

8.1

C.d

.UR

F4.

8F

unt.

YL

4.4

C.a

.YL

8.7

Phy

t.M

L4.

4C

.a.Y

L6.

5P

ru.M

L6.

6P

ru.Y

L6.

4C

.a.Y

L7.

8So

dium

C.d

.YL

30.0

C.d

.YL

18.3

C.d

.YL

24.7

Alb

.YL

26.2

Dom

b.Y

L21

.1E

uc.B

ark

20.9

Dom

bY

L15

.2E

uc.Y

L31

.1D

omb.

YL

20.3

Euc

.Bar

k17

.0C

.d.L

B13

.7E

uc.Y

L21

.3C

.d.Y

L17

.9P

ru.M

L7.

8C

.d.Y

L

P1: FYJ



14.5

Dom

b.Y

L20

.9M

ark.

YL

13.6

Euc

.YL

16.7

Alb

.YL

12.0

C.a

.YL

6.4

Stro

m.Y

L7.

9St

rom

.YL

6.5

C.a

.YL

10.9

Alb

.YL

8.6

C.a

.YL

10.2

C.a

.YL

6.4

C.a

.YL

8.7

Pru

.YL

6.3

Bos

.YL

6.6

Dom

b.Y

L6.

4O

lea

YL

10.0

Pru

.YL

8.0

Alb

.YL

3.9

Euc

.RF

6.4

C.d

UR

F7.

5D

omb.

YL

5.8

Mar

k.Y

L6.

0P

ar.Y

L5.

6M

ark.

YL

7.8

Fic.

natM

L6.

3M

agne

sium

C.d

.YL

30.7

C.d

.YL

24.9

C.d

.YL

22.6

Alb

.YL

30.0

C.d

.YL

16.7

Par

.YL

11.4

C.a

.YL

17.0

Pru

.YL

14.5

C.a

.YL

17.5

C.a

.YL

14.8

C.d

UR

F18

.3C

.a.Y

L12

.1D

omb.

YL

10.1

C.a

.YL

10.1

C.d

.YL

13.4

Dom

b.Y

L14

.0D

omb.

YL

10.6

Pru

.YL

7.9

C.a

.YL

13.4

Pru

.YL

9.8

C.a

.YL

8.7

Pru

.ML

9.9

Dom

bY

L7.

2A

lb.Y

L11

.5M

ark.

YL

8.4

C.d

UR

F5.

1A

lb.Y

L11

.2P

hyt.

ML

9.5

Par

.YL

8.5

Stro

m.Y

L6.

6P

ar.Y

L7.

0M

im.M

L10

.1C

.dU

RF

7.9

Fun

t.Y

L4.

8C

.d.L

B6.

1St

ryc.

YL

4.8

Bos

.YL

8.4

Fun

t.Y

L5.

7M

il.Y

L6.

3C

.a.Y

L9.

7P

otas

sium

C.d

.YL

35.4

C.d

.YL

32.2

C.d

.YL

28.5

Alb

.YL

35.8

C.d

.YL

20.3

Stro

m.Y

L8.

1C

.d.Y

L16

.8D

omb.

YL

15.3

Mar

k.Y

L15

.0C

.a.Y

L10

.2A

lb.Y

L13

.3P

ru.Y

L8.

2D

omb.

YL

9.8

C.d

.YL

7.7

C.a

.YL

11.3

Alb

.YL

14.7

C.a

.YL

10.8

Mar

k.Y

L8.

2C

.a.Y

L9.

0C

.a.Y

L8.

1M

ark.

Pet

8.6

C.a

.YL

7.6

Ole

aY

L9.

3P

ru.Y

L13

.1D

omb.

YL

9.8

Pru

.YL

6.8

C.d

UR

F8.

9P

hyt.

ML

5.4

Bos

.YL

7.7

Par

.YL

7.1

Mar

k.Y

L8.

4C

.a.Y

L7.

0A

lb.Y

L4.

4A

lb.Y

L5.

7C

.d.L

B7.

6St

ryc.

YL

5.2

Stro

m.Y

L7.

2P

ru.M

L7.

0D

omb

YL

7.3

Fic

Nat

ML

7.0

Cal

cium

C.a

.YL

32.4

C.a

.YL

28.2

C.a

.YL

25.7

C.a

.YL

22.1

C.d

.YL

18.9

C.a

.YL

19.2

C.a

.YL

32.4

C.a

.YL

18.2

C.d

.YL

25.1

C.d

.YL

20.8

C.d

.YL

19.2

Alb

.YL

17.0

Dom

b.Y

L7.

9E

uc.B

ark

11.7

C.d

.YL

11.3

Dom

b.Y

L12

.5D

omb.

YL

9.3

Euc

.Bar

k12

.0C

.dU

RF

16.1

Vin

esM

L9.

9M

ark.

YL

7.6

Pru

.ML

10.0

Ole

aY

L7.

1M

im.M

L10

.8C

.dU

RF

6.8

Pru

.YL

5.4

Alb

.YL

6.6

Phy

t.M

L6.

9B

os.Y

L7.

4P

ar.Y

L9.

9D

omb

YL

6.5

Pru

.YL

9.9

Mar

k.Y

L4.

7P

ru.M

L4.

6O

lea

Pet

.6.

2P

ru.Y

L6.

5P

ar.Y

L7.

2St

rom

.Pet

5.9

Par

.YL

6.1

Fic

Nat

ML

7.4

Not

e.A

lb=

Alb

izia

gran

dibr

acte

ata,

Blig=

Blig

hia

uniju

gata

,Bos=

Bos

quei

aph

ober

os,C

.a.=

Cel

tisaf

rica

na,C

.d.=

Cel

tisdu

rand

ii,C

hyr=

Chr

ysop

hyllu

msp

.,D

ios=

Dio

spyr

osab

yssi

nica

,Dom

b=

Dom

beya

muk

ole,

Euc=

Euc

alyp

tus,

Fic

nat=F

icus

nata

lens

is,

Fun

t=F

untu

mia

latif

olia

,Mar

k=

Mar

kham

iapl

atyc

alyx

,Mil=

Mill

ettia

dura

,Mim=

Mim

usop

sbag

shaw

ei,O

lea=

Ole

aw

elw

itsch

ii,P

ar=

Par

inar

iexc

elsa

,Phy

t=P

hyto

lacc

asp

.,P

ru=

Pru

nus

afri

cana

,Str

om=

Stro

mbo

sia

sche

ffler

i,St

ryc=

Stry

chno

sm

itis,

Tec=

Tecl

eano

bilis

).A

bbre

viat

ions

for

plan

tpar

tsin

clud

eM

L=

mat

ure

leav

es,Y

L=

youn

gle

aves

,LB=

leaf

buds

,Pet=

leaf

peti

oles

,U

RF=

unri

pefr

uit,

and

RF=

ripe

frui

t.

P1: FYJ



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.

REFERENCES

Altmann, S. A. (1998). Foraging for Survival: Yearling Baboons in Africa, University of ChicagoPress, Chicago.

Baranga, D. (1983). Changes in chemical composition of food parts in the diet of colobusmonkeys. Ecology 64: 668–673.

Barker, D., Fitzpatrick, M. P., and Dierenfeld, E. S. (1998). Nutrient composition of selectedwhole invertebrates. Zoo Biol. 17: 123–134.

Beck, J., Muhlenberg, E., and Fiedlerm K. (1999). Mud-puddling behavior in tropical butterflies:In search of proteins or minerals. Oecologia 119: 140–148.

Bell, F. R. (1995). Perception of sodium appetite in farm animals. In Phillips, C. J. C., and Chiy,P.C. (eds.), Sodium in Agriculture, Cantebury, UK, pp. 82–90.

Belovsky, G. E. (1981). A possible population response of moose to sodium availability. J.Mammal. 62: 631–633.

Blair-West, J. R., Coghlan, J. P., Denton, D. A., Nelson, J. F., Orchard, E., Scoggins, B. A., Wright,R. D., Myers, K., and Jungueira, C. L. (1968). Physiological, morphological, and behavioraladaptations to a sodium deficient environment by wild native Australian and introducedspecies of animals. Nature 217: 922–928.

Buss, D. H., and Cooper, R. W. (1970). Composition of milk from talapoin monkeys. FoliaPrimatol. 13: 196–206.

Chapman, C. A., and Chapman, L. J. (1997). Forest regeneration in logged and unlogged forestsof Kibale National Park, Uganda. Biotropica 29: 396–412.

Chapman, C. A., and Chapman, L. J. (1999). Implications of small scale variation in ecologicalconditions for the diet and density of red colobus monkeys. Primate 40: 215–232.

Chapman, C. A., and Chapman, L. J. (2002). Foraging challenges of red colobus monkeys:Influence of nutrients and secondary compounds. Comp. Biochem. Physiol. 133: 861–875.

Chapman, C. A., Chapman, L. J., Bjorndal, K. A., and Onderdonk, D. A. (2002). Applicationof protein to fiber ratios to predict colobine abundance on different spatial scales. Int. J.Primatol. 23: 283–310.

Chapman, C. A., Chapman, L. J., Cords, M., Gathua, M. J., Gautier-Hion, A., Lambert, J. E.,Rode, K. D.,Tutin, C. E. G., and White, L. J. T. (2002). Variation in the diets of Cercopithecusspecies: Differences within forests, among forests, and across species. In Glenn, M., andCords, M. (eds), The Guenons: Diversity and Adaptation in African Monkeys, PlenumPress, New York, pp. 325–350.

Chapman, L. J., Chapman, C. A., Crisman, T. L., and Nordlie, F. G. (1998). Dissolved oxygenand thermal regimes of a Ugandan crater lake. Hydrobiologia 385: 201–211.

Chapman, C. A., and Lambert, J. E. (2000). Habitat alteration and the conservation of Africanprimates: A case study of Kibale National Park, Uganda. Am. J. Primatol. 50: 169–186.

P1: FYJ



Chapman, C. A., Lawes, M. J., Naughton-Treves, L., Gillespie, T. R. (2003). Primate survival incommunity-owned forest fragments: Are metapopulation models useful amidst intensiveuse. In Marsh, L. K. (ed.), Primates in Fragments: Ecology and Conservation, KluwerAcademic/Plenum, New York, pp. 63–78.

Chiy, P. C., and Phillips, C. J. C. (1995). Sodium in ruminant nutrition, production, reproduction,and health. In Phillips, C. J. C., and Chiy, P. C. (eds.), Sodium in Agriculture, Cantebury,UK, pp. 107–144.

Conover, M. R. (1998). Perceptions of American agricultural producers about wildlife on theirfarms and ranches. Wildl. Soc. Bull. 26: 597–604.

Crissey, S. D., and Pribyl, L. S. (1997). Utilizing wild foraging ecology information to providecaptive primates with an appropriate diet. Proc. Nutr. Soc. 56: 1083–1094.

Cunningham-Rundles, S., and Ho Lin, D. (1998). Nutrition and the immune system of the gut.Nutrition 14: 573–579.

Delgiudice, G. D., Singer, F. J., Seal, U. S., and Bowser G. (1994). Physiological responsesof Yellowstone bison to winter nutritional deprivation. J. Wildl. Manage. 58: 24–34.

Dierenfeld, E. S., and McCann, C. M. (1999). Nutrient composition of selected species consumedby semi free-ranging lion-tailed macaques (Macaca silenus) and ring-tailed lemurs (Lemurcatta) on St. Catherines Island, Georgia, U.S.A. Zoo Biol. 18: 481–494.

Dorrestein, G. M., de Sa, L., Ratiarison, S., and Mete, A. (2000). Iron in the liver of animals inthe zoo: A pathologist’s point of view. In Nijboer, J., Hatt, J.-M., Kaumanns, W., Beijnen, A.,and Ganslosser, U. (eds.), Zoo Animal Nutrition, Filander Verlag, Furth, The Netherlands,pp. 291–299.

Faber, W. E., Pehrson, A., and Jordan, P. A. (1993). Seasonal use of salt blocks by mountainhares in Sweden. J. Wildl. Manage 57: 842–846.

Fox, L. M., Krausman, P. R., Morrison, M. L., and Noon, T. H. (2000). Mineral content ofSonoran pronghorn forage. Calif. Fish Game 86: 159–174.

Fraser, D. (1979). Aquatic feeding by the woodchuck. Can. Field Nat. 93: 309–310.Fraser, D., Chavez, E. R., and Paloheimo, J. E. (1984). Aquatic feeding by moose: Selection of

plant species and feeding areas in relation to plant chemical composition and characteristicsof lakes. Can. J. Zool. 62 : 80–87.

Hailey, A., and Coulson, I. M. (1996). Differential scaling of home range to daily movement intwo African tortoises. Can. J. Zool. 74: 97–102.

Hambidge, M. (2000). Human zinc deficiency. J. Nutr. 130: 1344–1349.Hellgren, E. C., and Pitts, W. J. (1997). Sodium economy in white-tailed deer (Odocoileus

virginianus). Phys. Zool. 70: 547–555.Hladik, C. M. (1978). Adaptive strategies of primates in relation to leaf-eating. In Montgomery,

G. C. (ed.), The Ecology of Arboreal Folivores, Smithsonian Institution Press, Washington,DC, pp. 373–395.

Holdo, R. M., Dudley, J. P., and McDowell, L. R. (2002). Environmental sodium availabilityand mineral lick use in the African elephant. J. Mammal. 83: 652–664.

Hotz, C., and Brown, K. H. (2001). Identifying populations at risk of zinc deficiency: The usesof supplementation trials. Nutr. Res. 59: 80–89.

Jackson, J. L., Lesho, E., and Peterson, C. (2000). Zinc and the common cold: A meta-analysisrevisited. J. Nutr. 130: 1512–1515.

Janson, C. H., and Chapman, C. A. (2000). Primate resources and the determination ofprimate community structure. In Fleagle, J. G., Janson, C. H., and Reed, K. (eds.),Primate Communities, Cambridge University Press, Cambridge, England, pp. 237–267.

Kaumanns, W., Hampe, K., Schwitzer, C., and Stahl, D. (2000). Primate nutrition: towards an in-tegrated approach. In Nijboer, J., Hatt, J.-M., Kaumanns, W., Beijnen, A., and Ganslosser,U. (eds.), Zoo Animal Nutrition, Filander Verlag, Furth, The Netherlands, pp. 91–106.

Krishnamani, R., and Mahaney, W. C. (2000). Geophagy among primates: Adaptive significanceand ecological consequences. Anim. Beh. 59: 899–915.

P1: FYJ



Lambert, J. E. (2000). Urine drinking in wild Cercopithecus ascanius: Evidence of nitrogenbalancing? Afr. J. Ecol. 38: 360–362.

Laska, M., Salazar, L. T. H., and Luna, E. R. (2000). Food preferences and nutrient compositionin captive spider monkeys, Ateles geoffroyi. Int. J. Primatol. 21: 671–683.

MacCracken, J. G., Vanballenberghe, V., and Peek, J. M. (1993). Use of aquatic plants bymoose—Sodium hunger or foraging efficiency. Can. J. Zool. 71: 2345–2351.

Marriott, B. M., Smith, J. C., Jacobs, R. M., Jones, A. O. L., and Altmann, J. D. (1996). Copper,iron, manganese, and zinc content of hair from two populations of rhesus monkeys. Biol.Trace Element Res. 53: 167–183.

Masters, D. G., Norman, N. C., and Dynes, R. A. (2001). Opportunities and limitationsfor animal production from saline land. Asian-Australasian. J. Anim. Sci. 14: 199–211.

Mattfield, G. F., Wiley, J. E., III, and Behrend D. F. (1972). Salt versus browse-seasonal baitsfor deer trapping. J. Wildl. Manage. 36: 996–998.

McDowell, L. R. (1985). Nutrition of Grazing Ruminants in Warm Climates, Academic Press,New York.

McDowell, L. R. (1992). Minerals in Animal and Human Nutrition, Academic Press, New York.McDowell, L. R. (1997). Minerals for Grazing Ruminants in Tropical Regions, University of

Florida, Gainesville.McNaughton, S. J. (1988). Mineral nutrition and spatial concentrations of African ungulates.

Nature 334: 343–345.Melack, J. M. (1978). Morphometric, physical and chemical features of the volcanic crater lakes

of western Uganda. Arch. Hydrobiol. 84: 430–453.Miles, P. H., Wilkinson, N. S., and McDowell, L. R. (2001). Analysis of Minerals for Animal

Nutrition Research, Department of Animal Sciences, University of Florida, Gainesville.Milewski, A. (2000). Iodine as a possible controlling nutrient for elephant populations. Pachy-

derm 28: 78–90.Miller, B. K., and Litvaitis, J. A. (1992). Use of roadside saltlicks by moose, Alces alces, in

Northern New Hampshire. Can. Field-Nat. 106: 112–117.Milton, K. (1996). Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler

monkey (Alouatta palliata) population in Panama. J. Zool. 239: 39–63.Milton, K. (1999). Nutritional characteristics of wild primate foods: Do the diets of our closest

living relative have lessons for us? Nutrition 15: 488–498.Milton, K. (2000). Back to basics: Why foods of wild primates have relevance for modern human

health. Nutrition 16: 480–483.Minatel, L., and Carfagnini, J. C. (2000). Copper deficiency and immune response in ruminants.

Nutr. Res. 20: 1519–1529.Nagy, K. A., and Milton, K. (1979). Aspects of dietary quality, nutrient assimilation and water

balance in wild howler monkeys (Alouatta palliata). Oecologia 39: 249–258.National Bureau of Standards (1982). U.S. Dept of Commerce. Standard Ref. Material 1572:

Citrus Leaves, Washington, DC.National Research Council (1978). Nutrient Requirements of Non-Human Primates, National

Academy Press, Washington, DC.National Research Council (1984). Nutrient Requirements of Domestic Animals, Nutrient Re-

quirements of Beef Cattle, 6th edn., National Academy of Sciences, Washington, DC.Naughton-Treves, L. (1998). Predicting patterns of crop raiding by wildlife around Kibale Na-

tional Park, Uganda. Con. Biol. 12: 151–168.NIST (1998). Standard Reference Material Catalog. NIST Publications 260, Gaithersburg, MD.Nicolosi, R. J., and Hunt, R. D. (1979). Dietary allowances for nutrients in nonhuman primates.

In Hayes, K. C. (ed.), Primates in Nutritional Research, Academic Press, New York.Oates, J. F. (1978). Water–plant and soil consumption by guereza monkeys (Colobus guereza):

A relationship with minerals and toxins in the diet? Biotropica 10: 241–253.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: Newevidence from West Africa. Ecology 71: 328–343.

P1: FYJ



Oftedal, O. T. (1991). The nutritional consequences of foraging in primates: The relationshipof nutrient intakes to nutrient requirements. Phil. Trans. R. Soc. London 334: 161–170.

Pletscher, D. H. (1987). Nutrient budgets for white-tailed deer in New England with specialreference to sodium. J. Mammal. 68: 330–336.

Power, M. L., Tardif, S. D., Layne, D. G., and Schulkin, J. (1999). Ingestion of calcium solutionsby common marmosets (Callithrix jacchus). Am. J. Primatol. 47: 255–261.

Ramirez, R. G., Haenlein, G. F. W., Trevino, A., and Reyna, J. (1996). Nutrient and mineralprofile of white-tailed deer (Odocoileus virginianus, texanus) diets in northeastern Mexico.Small Ruminant Res. 23: 7–16.

Robbins, C. T. (1993). Wildlife Feeding and Nutrition, Academic Press, New York.Ruel, M. T., and Bouis, H. E. (1998). Plant breeding: A long-term strategy for the control of

zinc deficiency in vulnerable populations. Am. J. Clin. Nutr. 68: 488–494.Sandstead, H. H., and Lofgren, P. A. (2000). Symposium: Dietary zinc and iron—Recent per-

spectives regarding growth and development. J. Nutr. 130: 345–346.Schwitzer, C., and Kaumanns, W. (2000). Feeding behaviour in two captive groups of black and

white ruffed lemurs (Varecia v. variegata), Kerr 1792. In Nijboer, J., Hatt, J.-M., Kaumanns,W., Beijnen, A., and Ganslosser, U. (eds.), Zoo Animal Nutrition, Filander Verlag, Furth,The Netherlands, pp. 119–130.

Silver, S. C., Ostro, L. E. T., Yeager, C. P., and Dierenfeld, E. S. (2000). Phytochemical andmineral components of foods consumed by black howler monkeys (Alouatta pigra) at twosites in Belize. Zoo Biol. 19: 95–109.

Skorupa, J. (1988). The Effect of Selective Timber Harvesting on Rain-forest Primates in KibaleForest, Uganda. PhD Dissertation, University of California, Davis.

Smith, W. H. (1976). Character and significance of forest tree root exudates. Ecology 57: 324–331.

Spelman, L. H., Osborn, K. G., and Anderson, M. P. (1989). Pathogenesis of hemosiderosis inlemurs: Role of dietary iron, tannin, and ascorbic acid. Zoo Biol. 8: 239–251.

Struhsaker, T. T. (1997). Ecology of an African Rain Forest: Logging in Kibale and the ConflictBetween Conservation and Exploitation, University Presses of Florida, Gainesville.

Sukumar, R. (1990). Ecology of the Asian elephant in southern India. II: Raiding habits andcrop raiding patterns. J. Trop. Ecol. 6: 33–53.

Sukumar, R., and Gadgil, M. (1988). Male–female differences in foraging on crops by Asianelephants. Anim. Behav. 36: 1233–1235.

Sun, C., Moermond, T. C., and Givnish, T. J. (1997). Nutritional determinants of diet in threeturacos in a tropical montane forest. Auk 114: 200–211.

Weeks, H. P., Jr., and Kirkpatrick, C. M. (1978). Salt preferences and sodium drive phenologyin fox squirrels and woodchucks. J. Mammal. 59: 531–542.

Weir, J. S. (1972). Spatial distribution of elephants in an African national park in relation toenvironmental sodium. Oikos 23: 1–13.

Wrangham, R. W., Conklin-Brittain, N. L., and Hunt, K. D. (1998). Dietary responses of chim-panzees and cercopithecines to seasonal variation in fruit abundance. I: Antifeedants. Int.J. Primatol. 19: 949–970.

Yeager, C. P., Silver, S. C., and Dierenfeld, E. S. (1997). Mineral and phytochemical influences onfoliage selection by the proboscis monkey (Nasalis larvatus). Am. J. Primatol. 41: 117–128.

Mineral Resource Availability and Consumption by Colobus in...

Documents

Transcript of Mineral Resource Availability and Consumption by Colobus in...