Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
1095-6433/03/$ - see front matter 
 2003 Elsevier Science Inc. All rights reserved.
doi:10.1016/S1095-6433(03)00084-9
Review
Micronutrient intakes of wild primates: are humans different?
Katharine Milton*
Department of Environmental Science, Policy and Management, Division Insect Biology, University of California, Berkeley,
CA 94720-3112, USA
Received 28 October 2002; received in revised form 16 February 2003; accepted 20 February 2003
Abstract
Low micronutrient intake is implicated in a diversity of human health problems, ranging from problems associated
with food insufficiency to those associated with food over-consumption. Humans are members of the order primates,
suborder anthropoidea, and are most closely related to the great apes. Humans and apes are remarkably similar
biologically. In the wild, apes and monkeys consume diets composed largely of plant foods, primarily the fruits and
leaves of tropical forest trees and vines. Considerable evidence indicates that the ancestral line giving rise to humans
(Homo spp.) was likewise strongly herbivorous (plant-eating). The wild plant parts consumed by apes and monkeys
show moderate to high levels of many minerals and vitamins. The estimated daily intake of specific minerals, vitamin
C and some other vitamins by wild primates is often quite high in comparison to intake levels of these same
micronutrients recommended for humans. Are the high micronutrient intakes of wild primates simply a non-functional,
unavoidable by-product of their strongly plant-based diets or might they actually be serving important as yet undetermined
immunological or other beneficial functions? A better understanding of the basis for this apparent difference between
humans and wild primates could help to clarify the range and proportions of micronutrients best suited for optimal
human development, health and longevity.

 2003 Elsevier Science Inc. All rights reserved.
Keywords: Vitamins; Minerals; Micronutrient requirements; Health; Diet; Monkeys; Apes
1. Introduction
Many current human health problems relate to
diet and much remains to be discovered about the
relationship between humans and their foods. At
some point, the biochemical foundations for many
human-food interactions will doubtless be better
understood. The multifactorial nature of the genet-
ic, cellular and physiological processes involved
 This paper is part of a collection of inter-disciplinary,
peer-reviewed articles under the Theme: ?Origin and Diversity
of Human Physiological Adaptability? invited by K.H.
Myburgh and the late P.W. Hochachka.
*Tel.: q1-510-642-8607.
E-mail address: kmilton@socrates.berkeley.edu
(K. Milton).
for each individual may, however, make
such understanding difficult (Williams, 1978;
Bengmark, 1998; Lampe, 1999).
Broadly speaking, many diet-related health prob-
lems fall into one of two categories. In one
category are problems particularly prevalent in
low-income nations?these problems often relate
to an insufficiency of higher quality foods, espe-
cially in infancy and childhood. Such insufficiency
is manifested, for example, in the high incidence
of linear growth retardation in young children in
low-income nations (Calloway et al., 1992; Mar-
torell, 1999; Berkman et al., 2002). In the other
category are diet-related health problems especially
prevalent in high-income nations?here many such
48 K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
problems relate not to food insufficiency but
rather to its oversupply andyor the over-consump-
tion of certain food types (Temple, 1994; Beng-
mark, 1998).
Critical examination of the many factors sug-
gested to relate to the multitude of current human
health problems stemming either from food inad-
equacy or food over-consumption is beyond the
scope of this paper. For this reason, I focus on one
factor strongly implicated in both sets of prob-
lems?namely, micronutrient intake. Using the
comparative approach I examine available data on
the content of various micronutrients in the foods
of wild primates and compare these estimates with
similar data on the micronutrient content of culti-
vated foods available in American super markets.
I then compare the probable daily intake of some
micronutrients by wild adult monkeys and apes
with recommended dietary allowances (RDAs)
suggested for adult Americans.
2. Background
Increasingly, clinical evidence suggests that
micronutrients are involved in vast array of impor-
tant biochemical processes. It has long been appre-
ciated that an adequate intake of certain
micronutrients relates to the prevention of classic
deficiency diseases such as pellegra, scurvy and
beriberi (Carpenter, 1981, 1986, 2000). An insuf-
ficiency of a particular micronutrient is also known
to lead to other specific health conditions (e.g.
lack of vitamin A and vision problems or blind-
ness, lack of iron and anemia). However, of late,
a new focus on micronutrients is occurring as
many other health problems in both low- and high-
income nations are now believed to relate, at least
in part, to an insufficiency of certain micro-
nutrients.
In low-income nations, for example, iron defi-
ciency is now regarded not only in terms of anemia
but also as a risk factor for cognitive defects in
school-aged children (Berkman et al., 2002). A
dietary study in Kenya designed to test the impact
of three different diet supplements (i.e. energy,
milk, meat) on cognitive development of school
children, showed children receiving supplemental
food with meat significantly outperformed all other
children on the Raven?s Progressive Matrix (Whal-
ey et al., 2002). This outcome was suggested to
relate, at least in part, to the many important
micronutrients in meat, particularly iron and zinc.
The protein in meat also improves the bioavaila-
bility of iron and zinc from grain and some other
plant foods?foods composing most of the diet in
such communities (Kikafunda et al., 1998; Whaley
et al., 2002). A study in Zanzibar likewise con-
cluded that low dose iron supplementation signif-
icantly improved language and motor development
of a community sample of rural preschool children
(Stoltzfus et al., 2001). Zinc supplementation in
Ugandan preschool children appeared to lower
infection rates (Kikafunda et al., 1998). Indonesian
prescholars given vitamin A fortification had a
significantly lower mortality rate and better growth
rate than prescholars not receiving such fortifica-
tion (Edmonds, 1999). Many studies examining
factors related to childhood health and develop-
ment have reached similar conclusions regarding
the importance of micronutrients (e.g. Calloway et
al., 1992).
In high-income nations on the other hand,
micronutrients are currently being viewed in a
somewhat different light. Here inadequate micro-
nutrient intake is of concern as it is hypothesized
to relate not only to traditional deficiency diseases
and developmental problems but also to DNA
damage, cancer and other degenerative diseases
(MacGregor, 1990; Block et al., 1992; Temple,
1994; Ames, 1989; Prasad et al., 1998; Victoroff,
2002). A recent review of studies examining the
role of dietary factors in cancer risk, for example,
determined that, overall, there is a considerably
higher cancer incidence among people who con-
sume fewer fruits and vegetables when compared
with those who consume the most (Ames and
Wakimoto, 2002). A dietary pattern rich in fruits
and vegetables also appears to play a protective
role in the prevention of cardiovascular disease
and stroke (Bazzana et al., 2002).
These studies ?firmly establish? (Rimm, 2002)
that the intake of fruit and vegetables lowers the
risk of chronic disease but they do not identify the
biological mechanisms responsible for this benefit
(Prasad et al., 1998; Ames and Wakimoto, 2002).
It is not clear which of the many chemical con-
stituents in fruits and vegetables may be respon-
sible for such protective effects. But there is strong
evidence that certain micronutrient deficiencies
cause DNA damage (Castro et al., 1992; Ames
and Wakimoto, 2002) and diets deficient in fruits
and vegetables are commonly low in folate, and
vitamins C and E, among other micronutrients
(Ames, 1989; Ames and Wakimoto, 2002).
49K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
Folate is an important component in DNA syn-
thesis while vitamins C and E are generally regard-
ed as potent antioxidants (Wardlaw and Insel,
1996; Ames and Wakimoto, 2002). It is currently
estimated that approximately two and a half billion
people are severely deficient in one or more
micronutrients, even though they get adequate or
marginally adequate macronutrients or calories
each day (Beachy et al., 2002). Most Americans
(i.e. 80% of children and adolescents, 68% of
adults; Krebs-Smith et al., 1995) take in low levels
of various micronutrients?levels lower than rec-
ommended by the National Cancer Institute and
National Research Council (Murphy et al., 1992;
Krebs-Smith et al., 1995) and likely insufficient
for optimal health and longevity (Ames and Wak-
imoto, 2002; Lewis et al., 1998). Underconsump-
tion of calcium, iron, magnesium, zinc, folate, and
vitamins B-6, A, E and C has been reported for
adults in the United States (US) (Murphy et al.,
1992; Lewis et al., 1998; Ames and Wakimoto,
2002).
As low micronutrient intake is implicated in
such a wide range of human health problems, it is
of interest to examine the micronutrient content of
a representative range of wild foods eaten by
monkeys and apes and estimate their micronutrient
intakes. As non-human primates, particularly the
great apes, are extremely similar to humans bio-
logically, it is logical to assume they should show
similar micronutrient requirements (Portman,
1970).
3. Diets of wild anthropoids
A wide variety of field studies provide data on
the daily diets of primates in the natural environ-
ment (Rodman, 1977; Wrangham, 1977; Milton,
1980; Calvert, 1985; Cords, 1987; Whiten et al.,
1991; Tutin et al., 1991; Matsumoto-Oda et al.,
1998). These studies show that both monkeys and
apes feed primarily on plant foods, eating moderate
to trace amounts of animal source foods (ASF),
generally insects (Harding, 1981). For example,
on average, African blue monkeys (Cercopithecus
mitis) and red-tailed monkeys (Cercopithecus
ascanius) are estimated to spend 73 and 75%,
respectively, of their daily feeding time on plant
foods (Cords, 1987) while for most baboon (Papio
spp.) species, this figure is placed at )90%
(Whiten et al., 1991). North Indian, forest-based
rhesus macaques (Macaca mulatta) are reported
to take ?almost the entire diet? from plant foods,
principally fruits (Lindburg, 1977). In the Neo-
tropics, plant foods are estimated to make up
)99% of the annual diet of wild howler monkeys
(Alouatta spp.) and spider monkeys (Ateles spp.)
(Milton, 1980, 1993a).
Among primates, the great apes are most closely
related to humans and data suggest that humans
and chimpanzees may have shared a common
ancestor as recently as 7?5 million years ago
(mya) (Wildman et al., 2002). The natural diets
of wild orangutans (Pongo pygmaeus) and gorillas
(Gorilla gorilla) are composed almost exclusively
()97%) of plant foods (Rodman, 1977; Calvert,
1985) while for common chimpanzees (Pan trog-
lodytes), this figure is placed at 88.5 to 095%,
depending on season and study site (Wrangham,
1977; Hladik, 1977; Stanford, 1999; Matsumoto-
Oda et al., 1998). Though chimpanzees occasion-
ally kill and eat vertebrate prey and often eat ants
or termites, ASFs make up only a small proportion
of the average chimpanzee diet, which is composed
largely of ripe fruits (Hladik, 1977; Wrangham,
1977; Tutin et al., 1991; Stanford, 1999; Matsu-
moto-Oda et al., 1998). All great apes can there-
fore be regarded as very strongly herbivorous
(plant-eating).
For wild primates as a class, fruit is by far the
most commonly consumed category of wild plant
food (Harding, 1981). Many primates also take
some proportion of the daily diet from leaves,
generally young leaves, but with a few exceptions
only large-bodied or digestively specialized pri-
mates (e.g. Colobinae) eat notable quantities of
leaves each day. Flowers, arils, seeds, bark, peti-
oles, rhizomes and other plant parts are also eaten
by some primates (Harding, 1981).
Most wild primates also eat moderate to trace
amounts of ASFs each day, generally insects or
other invertebrates and some species (e.g. chim-
panzees, capuchin monkeys, baboons) will capture
and eat smaller vertebrates. However, out of 131
primate species surveyed, none had ASFs as a
major dietary component (Harding, 1981). Though
ASFs can be an important source of micronutrients,
particularly B , B , iron and zinc, I confine my6 12
examination below to the plant food portion of the
wild primate diet. Any animal matter ingested
would only increase micronutrient intake estimates.
The plant-based dietary focus of apes and mon-
keys appears evolutionarily quite ancient. The
dentition of fossil apes more than 15 million years
50 K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
old indicates a plant-eating, primarily frugivorous,
way of life (Kay, 1977). There seems general
consensus that the ancestral form giving rise to
the human (Homo) lineage was likewise markedly
herbivorous, a fact supported by the sacculated
form of the modern human colon, the slow kinetic
pattern of ingesta turnover which characterizes
both humans and the great apes and the inability
of humans (and all other anthropoids) to synthe-
size vitamin C?a trait found in only a few other
highly herbivorous lineages (Milton and Jenness,
1987; Milton and Demment, 1988; Caton, 1999;
Caton et al., 1999).
4. Micronutrient content of wild primate foods
Primates are believed to have evolved in tropical
forests and even today most are highly arboreal.
Therefore, the plant foods available to them over
their long evolutionary history have been largely
the leaves, fruits and flowers of tropical forest
trees and vines. Remarkably little is known about
the micronutrient content of such wild foods. Table
1 presents some comparative data on mineral levels
of some wild fruit, leaf and flower species eaten
by free-ranging monkeys, apes and bats and culti-
vated fruits and vegetables eaten by Americans
and Samoans. As soil type and other environmental
conditions can greatly affect the chemical compo-
sition of plants, data from several locales are given
for the wild foods.
4.1. Minerals
Various wild plant foods compare favorably in
levels of some minerals with cultivated plant foods
(Table 1). Wild fruits from Panama, Venezuela,
Gabon, Cameroon and Samoa show higher average
values for calcium and phosphorous than cultivated
fruits from the US and Samoa. Wild fruits from
Panama, Cameroon and Samoa are also higher in
potassium than cultivated fruits from the US and
Samoa and higher in iron than cultivated fruits
from the US. Table 1 also presents comparative
estimates for 16 species of wild and 4 species of
cultivated fruits from American Samoa (Nelson et
al., 2000). All of the Samoan wild fruits, which
are eaten by bats, are similar in type and compo-
sition to those eaten by wild primates. Wild Samo-
an fruits differed significantly from cultivated
Samoan fruits in mean levels of copper, iron,
sodium and calcium (Nelson et al., 2000). Wild
Samoan fruits also showed more interspecific var-
iation in mineral content than cultivated Samoan
fruits.
Results are mixed for the mineral content of
wild leaves (and flowers) when compared with
those from cultivated foliar and other vegetable
foods. Wild leaves from Panama and Cameroon,
for example, average slightly higher calcium val-
ues relative to cultivated foods but wild leaves
from Venezuela and Gabon are lower in calcium
than similar cultivated foods. Cultivated leafy and
vegetable foods from the US are higher in phos-
phorous and potassium than wild leaves from any
site examined (Table 1).
Similar results have been found in other studies
in which wild fruits, leaves or other wild plant
parts eaten by humans were compared with locally
available, cultivated plant foods in the same food
category (Brand et al., 1983; Booth et al., 1992;
Kuhnlein and Turner, 1991). These data indicate
that wild plant foods of many types show moderate
to high values for various minerals relative to their
cultivated counterparts as well as high interspecific
variation for particular minerals within sites. This
latter feature is important because, for example,
though most wild plant foods at a given locale
may be low in a particular mineral, one or two are
likely to be unusually high. By eating a variety of
different plant foods each day (e.g. fruits and
leaves from a number of different species), a
characteristic feeding pattern of wild primates
(Milton, 1987), a monkey or ape is more likely to
get the optimal level of each micronutrient required
(Nagy and Milton, 1979; Milton, 1999a).
4.2. Vitamins
There appears to be little information on the
vitamin content of wild fruits and leaves from
tropical forest tree species eaten by wild primates.
One vitamin which has been fairly extensively
examined in wild foods is vitamin C or ascorbate.
Both leaves and fruits from wild plant species,
including tree species, have been examined for
ascorbate content in both tropical and temperate
locales (Jones and Hughes, 1983; Dash and Jen-
ness, 1985; Keshinro, 1985). This interest likely
stems from the fact that vitamin C is of particular
importance to humans. Unlike most mammals
which synthesize their own ascorbate internally,
all anthropoids, including humans, lack the enzyme
L-gulonolactone oxidase (GLO, EC 1.1.3.8),
51
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Table 1
Mineral content of wild and cultivated plant foods (mean"S.D.)
Ca P K Na Mg Fe Mn Cu
(mgyg dry wt.) (mgyg dry wt.) (mgyg dry wt.) (mgyg dry wt.) (mgyg dry wt.) (mgyg dry wt.) (mgyg dry wt.) (mgyg dry wt.)
Wild Panamaa
Leaves, young (6 species) 14.9"15.5 2.2"1.2 21.1"5.8 2.3"3.9 4.6"2.6 84.4"25.5 74"81 19.6"17.0
Fruits, ripe (2 species) 13.1"0.6 1.3"0.02 25.1"1.4 0.5"0 2.8"0.4 52.5"0.7 46.5"10.6 4.2"1.1
Fruits, immature (1 species) 13.3 2.5 23.3 0.6 6.2 183 79 15.1
Flowers (1 species) 3.0 2.7 39.6 2.7 4.3 59.0 4.0 22.7
Wild Venezuelab
Leaves (5 species) 2.9"0.7 2.8"0.6 ? ? ? ? ? ?
Fruits (9 species) 6.4"1.7 1.6"0.5 ? ? ? ? ? ?
Wild Gabonc
Leaves (5 species) (4 species Na) 2.7"1.1 1.9"0.5 13.8"2.2 3.3"1.8 ? ? ? ?
Fruits (8 species) (7 species Na) 3.2"2.2 1.2"0.5 11.7"4.0 1.3"0.5 ? ? ? ?
Flowers (2 species) 3.4"1.5 2.9"0.01 19.3"7.6 1.9"1.3 ? ? ? ?
Wild Cameroond
Leaves (5 species) 12.3"11.5 1.8"0.8 17.2"8.5 0.2"0.1 2.4"1.6 260"200 342"131 14.0"7.0
Fruits (6 species) 3.5"4.5 1.3"0.9 16.0"11.0 0.1"0.2 1.4"0.6 250"469 120"147 12.0"11.0
Wild Samoae
Fruits (16 species) 5.1"3.7 ? 20.0"9.0 1.5"0.9 3.3"1.3 86.9"63.3 10.6"6.4 9.0"3.6
Cultivated Samoaf
Cultivated fruits (4 species) 1.2"0.9 ? 20.8"2.9 0.2"0.1 2.5"0.6 8.3"6.3 8.5"2.9 5.0"2.1
Cultivated USg
Foliar cultivars (11 species) 11.2"7.8 4.9"1.8 34.9"17.6 ? ? 188.3"124.9 ? ?
Other cultivars (10 species) 3.3"2.8 5.9"2.6 22.5"2.6 ? ? 81.0"32.6 ? ?
Root cultivars (3 species) 1.3"1.0 2.5"0.8 14.2"5.9 ? ? 33.0"12.3 ? ?
Cultivated fruits (20 species) 1.3"0.8 1.1"0.3 13.0"4.6 ? ? 34.8"14.6 ? ?
Ca, calcium; P, phosphorous; K, potassium; Na, sodium; Mg, magnesium; Fe, iron; Mn, manganese; Cu, copper.
Nagy and Milton (1979).a
Oftedal (1991).b
Hladik (1977).c
Calvert (1985).d
Nelson et al. (2000).e
Nelson et al. (2000).f
USDA, Nutritive Value of Foods, 10th ed., 1981.g
52 K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
Table 2
Ascorbic acid content of plant parts from different locales
Locale, kind of samples Ascorbic Acid (mgy100 g fresh wt.)
No. Species No. Specimens Mean* S.D. Median Range Ref.
Panama
Foliage 16 40 96.3 92.6 78 7?585 ?
Foliage** 16 39 83.8 48.6 76 7?212 ?
Fruit 10 14 62.4 72.0 37 6?268 ?
Fruit*** 10 13 46.5 42.6 33 6?128 ?
Flowers 3 4 16?180 ?
Venezuela
Foliage**** 4 197.5 86.1 119?300 q
Fruit juice**** 4 85.0 32.6 55?118 q
Nigeria
Fruit unusual 10 81.7 81.9 12?260 |
Fruit common 8 73.6 88.5 17?289 |
Wales (UK)
Foliage 213 ca. 2500 161.7 109.4 ?
New South Wales (Australia)
Foliage (evergreen) 10 10 198.3 81.8 102?307 /
Foliar cultivars 10 57.3 26.2 ?
Plant food of
hunter?gatherers 27 26.8 D
*Mean of all specimens for Panama material, mean of species for others. **Very young leaves of F. yoponensis excluded; ***Unripe
fruit of F. yoponensis excluded; ****Lemon, orange, mango, papaya. ? Milton and Jenness, 1987. q Marquez and Baumrucker, 1957.
| Keshinro, 1985. ? Jones and Hughes, 1983. / Dash and Jenness, 1985. D Eaton and Konner, 1985. (Reprinted from Experientia 43,
Milton, K. and Jenness, R. Ascorbic acid content of neotropical plant parts available to wild monkeys and bats, pp. 339?342, 1987
with permission from Birkhauser Publishing).
which catalyzes the final step in ascorbate synthe-
sis from glucose. For this reason, monkeys, apes
and humans must ingest adequate vitamin C in the
diet (Milton and Jenness, 1987).
Data on ascorbate values of fruit and leaves
from wild and cultivated plant species from various
locales are presented in Table 2. The mean for
ascorbate values for the edible portion of ten
Nigerian wild fruit species was higher than that
for eight commonly consumed Nigerian cultivated
fruit species (Keshinro, 1985). Panamanian fruits
routinely eaten by wild monkeys contain notable
amounts of ascorbate (Milton and Jenness, 1987).
One species of Panamanian wild fig, Ficus yopo-
nensis, showed an ascorbate level in fruits (2340
mg ascorbate per 100 g fresh wt.) that appears to
be one of the highest reported (Milton and Jenness,
1987). Wild Panamanian leaves averaged a higher
ascorbate content than cultivated fruit juices and
wild leaves, both tropical and temperate, are excel-
lent sources of ascorbate, better, for example, than
cultivated leafy vegetables (Jones and Hughes,
1983; Booth et al., 1992).
Because vitamin K is involved in photosynthe-
sis, wild leaves should also be a good source of
vitamin K (Booth et al., 1992). Many wild fruits
eaten by monkeys and apes have brilliant yellow
or orange flesh, at times oily flesh (e.g. Palmae),
and would appear to be good sources of bioavail-
able carotenoids (Booth et al., 1992; Pee et al.,
1998). Though wild plant food sources of primates
do not appear, as yet, to have been analyzed for
other vitamins, it is likely that many of the fruits,
arils, seeds, leaves, flowers and buds wild monkeys
and apes consume are good sources of various
other micronutrients.
Worthington (2001) recently carried out an
extensive review of the nutrient content of organic
vs. conventional crops. Similar to many results for
wild plant foods, her results showed that organic
plant foods contained significantly more iron, mag-
nesium, phosphorous and vitamin C than conven-
tional crop foods.
5. Micronutrient requirements and intake by
wild primates
5.1. Requirements
As pointed out by Nicolosi and Hunt (1979),
due to the many variables involved, it is difficult
53K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
Table 3
Estimated daily mineral intakes of wild howler monkeys and humans (all units mg)
Mineral Estimated Total daily Total daily Estimated assim. rate Estimated assim.
intake-adult intake-7 kg RDA-adult per kilogram- rate per
wild howler adult wild human male adult kilogram-
monkey howler wild howler adult human
per kg per day monkey monkey male
Calcium, mg 653 4571 800 20 4
Phosphorus, mg 104 728 800 6 9
Potassium, mg 917 6419 1600?2000 393 27
Sodium, mg 26 182 500 12 16
Chloride, mg 254 1778 750 102 24
Magnesium, mg 189 1323 350 9 2
Iron, mg 5.5 38.5 10.0 0.92 0.45
Manganese, mg 2.6 18.2 2.0?5.0 0.01 ?
Modified from materials in Nagy and Milton (1979). Intakes and assimilation estimates derive from feeding trials and observations
of wild howler monkeys eating a typical leaf and fruit diet. See Nagy and Milton (1979) for details of feeding trials and analytical
protocols. Assimilation rates in humans estimated from assimilation percentages given by the National Research Council (1968),
Passmore et al. (1974) and Williams (1974).
to be precise about the nutrient requirements of
non-human primates and this is particularly true
in the case of micronutrients. Despite the important
and varied role of minerals in physiological pro-
cesses, few studies have concerned themselves
with the mineral requirements of non-human pri-
mates (Nicolosi and Hunt, 1979). Vitamin requi-
rements for non-human primates have been
somewhat better investigated, but are still not well-
defined for most vitamins. Such studies generally
establish the minimum level of a particular mineral
or vitamin required by a given primate species to
prevent deficiency disorders rather than determine
the optimal level. Perhaps for this reason, estimates
for both minerals and vitamins for non-human
primates often appear to err on the side of caution,
being higher than would be predicted by body
weight (Portman, 1970). Deficiency studies show
that non-human primates require an intake of many
of the same minerals and vitamins as humans but
it seems difficult to specify daily requirements.
Portman (1970), Kerr (1972), Nicolosi and Hunt
(1979) and Oftedal (1991) offer summaries of
data available on recommended nutrient intake
levels for non-human primates, including micro-
nutrients.
5.2. Intake
The daily intake of particular micronutrients by
wild primates can be crudely estimated from
detailed information on feeding behavior in the
natural environment and knowledge of the micro-
nutrient content of important wild foods. For
example, data on the feeding behavior of wild
adult howler monkeys in Panama, in combination
with analyses of some wild foods, allow an esti-
mate of their daily intake of some minerals. As
shown in Table 3, howler monkeys appear to take
in very high levels of many minerals each day
relative to RDAs suggested for humans (Nagy and
Milton, 1979). Values for the calcium, phospho-
rous and potassium content of important wild fruits
in the diet of Gabonese chimpanzees (Table 1), in
combination with my conservative estimate of the
daily fruit intake of adult wild chimpanzees (i.e.
700 g dry wt.) indicate that these apes take in
high levels of all three minerals. These estimates
relate to only the fruit portion of the diet?
chimpanzees also eat other plant parts and some
ASFs (Hladik, 1977; Wrangham, 1977). By anal-
ogy, it would appear that most free-ranging mon-
keys and apes eating wild fruits and leaves of
similar mineral content to those in Table 1 take in
high levels of many minerals each day.
Wild primates also take in notable levels of
vitamin C (ascorbate). A 7 kg adult wild howler
monkey in Panama, for example, is estimated to
consume approximately 600 g of fruit and 400 g
of leaves, wet weight per day. With the average
ascorbate content given in Table 2, intake is
estimated at 279 mg of ascorbate from fruit and
335 mg from leaves for a total of 614 mg or 88
mgykgyday. Wild Panamanian spider monkeys,
which average 7 kg when adult, eat considerably
more fruit per day than howler monkeys, some
54 K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
1600 g wet wt.yday. This would furnish 106 mgy
kgyday of ascorbic acid or a total of 744 mg of
ascorbate per day (Milton and Jenness, 1987) and
spider monkeys also eat some leaves each day.
Bourne (1949) estimated that wild gorillas con-
suming approximately 9 kg of wild ?green foods?
per day might take in more than 4 g of ascorbate.
Similar high ascorbate intake seems unavoidable
for wild chimpanzees and orangutans with their
strong focus on ripe fruits in the diet as well as
for many monkeys. Mammals from other plant-
eating orders are likewise reported to take in or
even require very high levels of ascorbate each
day. Levine (1986), for example, pointed out that
guinea pigs (like anthropoids a lineage that
requires a dietary source of vitamin C), needed
approximately 10 times more vitamin C to main-
tain general health than was required to prevent
scurvy.
The current RDA for vitamin C for the average
adult American is approximately 1 mgykgyday.
Thus a 70 kg adult would take in approximately
70 mg of vitamin C per day?far less than a 7 kg
wild howler or spider monkey would be taking in
per kilogram of body weight per day. Humans
therefore appear to take in far less ascorbate per
day than most wild primates, including similar-
sized wild apes.
6. Micronutrient levels offered captive primates
What micronutrient levels are offered to captive
non-human primates? Bilby (1968) presented com-
parative data on levels for several minerals offered
captive primates. There was notable variation. For
example, the mean calcium level per kilogram
body weight for monkeys at the London Zoo was
34 mg (range 26?120 mg) while 400 mgykg was
offered captive monkeys in Purina chow and 112
mgykg was offered captive monkeys at Monkey
Hill (Bilby, 1968).
In terms of ascorbate intake, a level of 0.5?1.0
mg of ascorbateykgyday, is suggested for captive
rhesus monkeys (M. mulatta) and 7.5?10 mg of
ascorbateykgyday for captive squirrel monkeys
(Samiri scuriius Nicolosi and Hunt, 1979). Port-
man (1970) suggests 25 mgykgyday of ascorbate
for captive non-human primates in general.
Kallman (1989) calculated the daily intakes per
kilogram body weight for 15 micronutrients for a
7 kg monkey consuming a commercial chow diet
and compared these estimates to human RDAs for
a 70 kg adult male. The mean of the ratios of
monkey intake per kilogram body weight to rec-
ommended human intakes per kilogram body
weight for the same 15 micronutrients was 23?
on average, the chow-fed monkeys were offered
23 times as much of a given micronutrient per
kilogram body weight in chow as was recom-
mended for an adult human male (Kallman, 1989).
No specific studies had been carried out to deter-
mine micronutrient levels for the monkey chow?
rather a safety factor had been added to minimum
estimates derived from deprivation or other studies
and present-day levels had resulted (Kallman,
1989).
7. Discussion
It seems unlikely, though not impossible, that
humans differ from other anthropoids in micronu-
trient requirements (with body mass and other
variables held constant). Humans, apes and mon-
keys are known to differ in some aspects of
nutrient requirements (e.g. dietary requirement for
vitamin D by Neotropical primates; Nicolosi and3
Hunt, 1979) and nutrient-associated physiology
(e.g. serum lipoprotein profiles; Nelson et al.,
1984). Regardless, it is the case that both wild
and captive non-human primates appear to take in
very high levels of some micronutrients relative to
human RDAs. These levels do not appear harmful
to the non-human primates?in the case of captive
primates eating chow diets, such levels are regard-
ed as ?optimal? (Kallman, 1989) and in the case
of wild primates, such daily levels are the norm.
Yet potential risks or no obvious benefits are
believed to be associated with high intakes of
some micronutrients by humans (Victoroff, 2002).
For example, data suggest that the human body
becomes saturated with vitamin C at intakes great-
er than approximately 150 mgyday (Wardlaw and
Insel, 1996) and that excess ascorbate is excreted
from the body. A high intake of vitamin C can
cause various health problems for humans includ-
ing stomach inflammation and diarrhea. Perhaps
for this reason, at megadose intakes of vitamin C,
the human body is suggested to develop enzyme
systems that rapidly metabolize ascorbate (War-
dlaw and Insel, 1996). Yet, as noted, guinea pigs,
which, like anthropoids, obtain their ascorbate
from dietary sources, require a daily intake of
ascorbate 10 times higher than that needed to
prevent scurvy to remain in good health. Animals
55K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
that synthesize their own ascorbate (almost all
mammals other than anthropoids, guinea pigs and
few others), often make it in very large amounts.
A hog produces 8 g of ascorbate per day though
it is not known what benefit this high synthesis
provides. (Wardlaw and Insel, 1996). As ascorbate
synthesis incurs a cost to the producer, it would
seem that such high synthesis would not take place
if the end product were not of value to the animal
producing it.
Several explanations, that are not mutually
exclusive, can be suggested to account for the
apparent difference in micronutrient intakes rec-
ommended for humans and those of non-human
primates.
(1) A high intake of certain micronutrients by
wild primates may be an unavoidable by-product
of their heavily plant-based diets. Here the argu-
ment would be that high micronutrient intake
occurs because it cannot be avoided and non-
human primate physiology has adapted to this
?superfluous? micronutrient load. In this explana-
tion, high micronutrient levels would be regarded
as a non-functional, unavoidable by-product of the
typical wild primate diet.
(2) Micronutrients in plant parts eaten by wild
primates may have low bioavailability. Thus what
looks like a very high intake might in fact just net
a sufficiency for the primate feeder. Experimental
data show, for example, that wild howler monkeys
are poor assimilators of various minerals in their
wild plant diets (Table 3). They appeared to
assimilate only approximately 3?4% of the calci-
um and magnesium, 6% of the phosphorous and
15% of the iron in the wild foods offered them in
feeding trials in Panama (Table 3; Nagy and
Milton, 1979). Such estimates are lower than those
for various other non-primate, plant-eating verte-
brates (Nagy and Milton, 1979).
(3) Though assimilation estimates for wild
howler monkeys are low, this is relative to the
very large quantities of particular minerals animals
take in each day in their wild plant foods. Howlers
actually assimilate considerably more of some
minerals per unit mass than adult humans (Table
3). For example, though assimilating only 20 mg
of calcium per kilogram body weight from their
wild foods (Table 3), a 7 kg adult howler monkey
would assimilate an estimated 140 mg of calcium
per day. A 70 kg adult human male (with an
estimated assimilation efficiency for dietary calci-
um of f35% and taking in the RDA of 800 mg)
assimilates 4 mg of calcium per kilogram of body
weight per day or a total of 280 mg. For its
metabolic body weight, a 7 kg howler monkey
(metabolic body wt.s4.3 kg) is assimilating
approximately 3 times as much calcium per kilo-
gram per day as a 70 kg adult human male
(metabolic body wt.s24.2 kg). Captive juvenile
rhesus macaques (M. mulatta) 01 year of age,
fed prepared rations containing 166 mg calciumy
kgyday stored an estimated 80 mgykgyday, show-
ing an assimilation efficiency of almost 50%
(Greenberg, 1970). For a 3 kg juvenile monkey
this would be a total of 240 mg of calcium
assimilated per day?in other words, the captive 3
kg juvenile monkey is assimilating almost as much
calcium per day as the 70-kg adult human male.
Unlike most other monogastric primates, howler
monkeys eat a high percentage of tree leaves each
day (Milton, 1980, 1993b). Wild leaves are often
protected against consumption by herbivore feed-
ers by distasteful or potentially harmful allelo-
chemicals?some of which are known to reduce
the availability of nutrients or are energetically
costly to detoxify (Milton, 1979, 1993b; Marriott,
2000). Unlike howler monkeys, most wild pri-
mates (excluding digestively specialized forms
such as the Colobinae) tend to fill up on ripe fruits
rather than leaves. As edible fruit pulp is elaborat-
ed by trees to attract seed dispersal agents such as
monkeys and apes, the bioavailability of micro-
nutrients in ripe fruits is predicted to be higher on
average than values for leaves.
It is the case, however, that wild plant foods
tend to be higher in potentially toxic or digestibi-
lity-reducing chemicals than cultivated plant foods.
High micronutrient intakes by wild primates could
function to lower potentially harmful effects of
some chemicals present in wild foods. Vitamins C
and E, for example, are a potent antioxidants which
should facilitate the metabolism or excretion of
undesirable plant compounds (e.g. phenols, ter-
penes; Dash and Jenness, 1985; Milton and Jen-
ness, 1987). In humans and guinea pigs, a
deficiency of ascorbate leads to reduced ability to
detoxify foreign chemicals (Dash and Jenness,
1985). As humans now eat cultivated plant foods,
the argument would be that they simply do not
require similar high levels of micronutrients as
their dietary conditions have altered and they no
longer have to deal with high levels of undesirable
constituents in wild foods.
56 K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
However, numerous novel chemical compounds
occur in human foods today, compounds which
differ from the plant toxins, tannins and other
natural environmental hazards wild primates have
apparently developed means to deal with during
their long evolutionary association with a wild
plant food diet. Most humans today are also
exposed to a wide array of air pollutants and other
chemical substances new to their biology, which
may require detoxification or call for enhanced
immunological or other defenses. Ironically,
humans may require high levels of antioxidants
and other micronutrients today to help counter the
effects of these new environmental hazards (but
see Ames and Gold, 1997).
8. Conclusions
Comparative data suggest that wild primates
take in higher levels of various vitamins and
minerals each day than those suggested for
humans. In the fresh plant foods monkeys and
apes eat, unlike fortified foods or supplements,
each nutrient is embedded in its natural organic
matrix, permitting normal synergistic, additive or
inhibitory biochemical effects to occur (Lampe,
1999; Prasad et al., 1998; Thompson et al., 2002;
Marriott, 2000). It may be normal for human as
well as ape and monkey blood and body tissues
to be saturated continuously with many of the
vitamins and minerals common in wild plant foods
and for large quantities to be flushing continuously
through the body (Bourne, 1949). This may pro-
duce quite different physiological benefits than the
short-term oxidative or other effects derived from
vitamin (Moller and Loft, 2002) or mineral sup-
plements or from generally low levels of many
micronutrients in the body due to inadequate die-
tary sources.
The suggestion that modern humans (and all
living humans are anatomically modern Homo
sapiens sapiens) increase their daily intake of fresh
fruits and vegetables seems sound even if we were
to base this recommendation purely on our knowl-
edge of the probable foodways of pre-human
ancestors and the present-day diets of wild apes
and monkeys. It seems unlikely that consuming
more lean meat or other ASF each day at the
expense of fresh fruits and vegetables would pro-
vide the same health benefits for the average adult
westerner. This is not to imply that humans should
eat like apes. Over evolutionary time, the human
gut has come to differ in certain respects from the
guts of extant apes and no longer appears suited
to large quantities of indigestible plant material
(Milton, 1986, 1987, 1993b, 1999b, 2002). For
this reason, all modern humans must eat higher
quality diets than all great apes (Milton, 1986,
1987, 1993b, 1999b, 2002).
In high-income nations at present, the general
human tendency to upgrade and improve dietary
quality has been carried to a new extreme as
numerous foods are now refined and condensed to
levels unimaginable to human populations even as
recently as 100 years ago. All daily energy requi-
rements can now be met with a relatively small
amount of food. Unfortunately, many individuals
in high-income nations tend to fill up each day on
these highly refined, energy-dense foods, foods
often demonstrably low in many micronutrients
relative to similar unrefined foods, (Temple, 1994;
Bengmark, 1998). For this reason, it is not sur-
prising that problems associated with low micro-
nutrient intake occur today in high-income nations
(Murphy et al., 1992; Lewis et al., 1998; Ames
and Wakimoto, 2002).
In low-income nations in contrast, millions of
people rely for most of their daily energy on a
single grain cultivar. These important cereal foods,
analogous to over-refined foods in high-income
nations, provide largely energy to the consumer.
However, in striking contrast to refined western
foods, cereal foods typically are less concentrated
volumetrically. Small children in particular, with
their characteristic human gut proportions and food
transit times but accelerated requirements for ener-
gy and nutrients would be hard pressed to meet
nutritional requirements on such foods, even if
these were available in unlimited quantity (Milton,
1999b, 2002). For this reason, ASF, which gener-
ally are highly digestible and also macro- and
micronutrient dense, are of particularly strong pos-
itive value to young children in such dietary
circumstances (Milton, 1999b; Whaley et al.,
2002). Cereal foods can then be used primarily as
an energy source.
The current dietary situation for many humans
in both high- and low-income nations does not
seem compatible with human biology. Human
biology evolved initially in conjunction with the
quality and anti-quality components of a pre-
human, largely wild plant-based diet. Human evo-
lution marked a departure from the pre-human
dietary pattern in that ASFs from vertebrates as
57K. Milton / Comparative Biochemistry and Physiology Part A 136 (2003) 47?59
well as new modes of food processing (both of
which up-graded dietary quality and thereby
reduced the total volume of food needed per day
to meet nutrient requirements) became the norm
(Milton and Demment, 1988; Milton, 1993b,
1999a). However, these adaptations in the human
lineage appear to relate more to the physical
properties of foods than their chemical properties.
For this reason, humans and great apes likely still
require the same micronutrients in the diet?they
just use different dietary strategies to obtain them.
Though the bioavailability of micronutrients to
wild primates is almost totally unstudied, a high
intake of various micronutrients (e.g. vitamins C
and E, provitamin A, calcium) appears to be the
norm. The difference between the estimated intake
of certain micronutrients by wild primates and
humans is striking. This difference is of particular
interest today because a large number of recent
studies strongly indicate health benefits to humans
from increasing amounts of fresh fruits and vege-
tables in the diet (Block et al., 1992; Temple,
1994; Ames and Wakimoto, 2002). A better under-
standing of the possible health implications of
such intake differences seems imperative due to
the strong biological similarity of humans to other
higher primates and the growing realization that
micronutrients may play far more important roles
in human development, health and longevity than
formerly have been appreciated.
Acknowledgments
I am particularly grateful to the late Dr P.W.
Hochachka, former Co-Editor of the Journal of
Comparative Biochemistry and Physiology who,
in collaboration with Dr Kathy Myburgh, envi-
sioned a thematic issue of CBP on the origin and
diversity of human physiological adaptability and
invited me to be a possible contributor.
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