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YEARBOOK OF PHYSICAL ANTHROPOLOGY 40:171–200 (1997)

Current Evidence for Self-Medication in Primates:
A Multidisciplinary Perspective
MICHAEL A. HUFFMAN
Primate Research Institute, Kyoto University, Aichi, Japan

KEY WORDS
primates; parasites; phytochemistry; plantselection; species comparison; zoopharmacognosy
ABSTRACTThe study of self-medication in non-human primates sheds
new light on the complex interactions of animal, plant and parasite. A variety
of non-nutritional plant secondary compounds and nutrient-poor bark is
found in the primate diet, but little is yet known about the possible medicinal
consequences of their ingestion. Recent studies of the African great apes
support a hypothesis in progress that the non-nutritional ingestion of certain
plant species aid in the control of parasite infection and provide relief from
related gastrointestinal upsets. Detailed behavioral, pharmacological andparasitological investigations of two such behaviors, bitter pith chewing andleaf swallowing, have been conducted on three East African chimpanzee
populations, but they are now known to occur widely among all chimpanzee
subspecies, as well as bonobos and lowland gorillas. For both bitter pithchewing and leaf swallowing, selection of the same plant species tends tooccur among neighboring groups of same ape species. These local cultural
traditions of plant selection may be transmitted when females of the same
species transfer into non-natal groups. However, selection of the same plant
species or species of related plant genera by two sympatric ape species or
between regional populations of great ape subspecies strongly suggests a
common criteria of medicinal plant selection. This and the intriguing observation that the same medicinal plant is selected by apes and humans withsimilar illnesses provide insight into the evolution of medicinal behavior inmodern humans and the possible nature of self-medication in early hominids.
The occurrence of these and other speci• c self-medicative behaviors, such as
fur rubbing and geophagy, in primates and other animal taxa suggest theexistence of an underlying mechanism for the recognition and use of plants
and soils with common medicinal or functional properties. Yrbk Phys
Anthropol 40:171–200, 1997. � 1997 Wiley-Liss, Inc.

In recent years a growing body of evidence
has given a burst of momentum to the studyof self-medication in animals, often called‘zoopharmacognosy’ (Glander, 1994; Huffman and Wrangham, 1994; Rodriguez andWrangham, 1993). The basic premise of zoopharmacognosy is that animals utilize plantsecondary compounds or other non-nutritional substances to medicate themselves.
Among primatologists a major focus ofconcern about plant secondary compounds

in the diet has been on how and why primates can cope with their presence (Glander, 1975, 1982; Hladik, 1977a,b; Janzen,
1978; McKey, 1978; Milton, 1979; Oates,
1977; Oates et al., 1977, 1980; Wrangham
and Waterman, 1981). An extreme case inpoint is the golden bamboo lemur (HapaleCorrespondence to: Michael A. Huffman, Section of Ecology,
Primate Research Institute, Kyoto University, Kanrin, Inuyama,
Aichi 484 Japan. E-mail: huffman@pri.kyoto-u.ac.jp

� 1997 WILEY-LISS, INC.

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YEARBOOK OF PHYSICAL ANTHROPOLOGY

mur aureus) of Madagascar, which is noted
to consume over 12 times the lethal adultlemur dose of cyanide in a day, without ill
affect (Glander et al., 1989). The cyanide
comes from the tips of a bamboo species,
Cephalostachyum sp. (Gramineae), consumed as part of the lemurs’ daily diet atcertain times of the year (Glander et al.,1989). In this case, the cyanide is thought tobe detoxi• ed mostly in the liver (Westly,1980). Herbivores are able to detoxify anumber of different compounds but theirpresence in sought after plants does have asigni• ca nt effect on feeding strategies (cf.
Freeland and Janzen, 1974).
One of the challenges and difficulties ofinterpreting self-medication is distinguishing between possible indirect medicinal bene• t s derived from secondary compound richplants that are assumed to be ingested fortheir nutritional value vs. limited and situation speci• c ingestion of items that areprocessed solely for their medicinal properties. Even in traditional human societies,
the difference between food and medicine
may not always be so clear. This is exempli• ed by a Japanese saying ‘‘ishoku dougen’’——which directly translated means‘‘medicine and food are of the same origin.’’ Acase in point is the fact that some of themore traditional spices and condiments ofdaily Asian cuisine, such as marine algae,
ginger root and herbs, contain importantsources of anti-tumor agents (Murakami etal., 1994, 1996; Ohigashi et al., 1992) which
may also play an important role in suppressing viral and parasite infections.
Parasites can cause a variety of diseases
which affect the overall behavior and reproductive • t ness of an individual (e.g. Hart,
1990; Holmes and Zohar, 1990). Therefore
the need to counteract such pressure should
be great (cf. Allison, 1982; Toft et al., 1991).
The effects of parasitosis on the host and thehost’s response to infection is undoubtedly
the product of a long evolutionary process(cf. Anderson and May, 1982; Barnard andBehnke, 1990; Behnke, 1987; Brooks andMcLennan, 1993; Ewald, 1994; Futuyma and
Slatkin, 1983; Hamilton, 1964a,b; Hamilton
and Zuk, 1982; Price, 1980). Janzen (1978)• rs t suggested the possibility that the incidental ingestion of secondary plant com-[Vol. 40, 1997

pounds by non-human primates and otheranimals may help to combat parasites.
Recent evidence from the African great
apes, however, suggests that certain plants
are ingested, not incidentally, but directly
for their signi• ca nt medicinal value. Theseobservations provide the clearest evidence
for self-medication thus far. Perhaps due toour phylogenetic closeness, humans andchimpanzees even select some of the sameplants when displaying similar symptoms of
illness (Huffman et al., 1996a). Unquestionably, these implications of self-medicative
behavior are of extreme interest when considering the evolution of medicinal habitsfrom the great apes to early hominids andmodern humans. The hypothesis currently
being developed from these investigations isthat the behaviors aid in the control ofintestinal parasites and/or provide relief
from related gastrointestinal upset.
The evidence for self-medication by African great apes includes the infrequent intake of plant species which are not a regularpart of the diet (Huffman and Seifu, 1989;
Wrangham and Nishida, 1983; Wrangham
and Goodall, 1989), a habit of ingestion
which provides no nutritional bene• t(Wrangham and Nishida, 1983; Huffman
and Seifu, 1989), restriction of plant use toseasons or other periods associated withhigh risk of parasitic infection (Huffman etal., 1990, 1997; Kawabata and Nishida, 1991;
Wrangham, 1995), illness or parasite infection of the individual at the time of ingestionof a putative medicinal plant (Huffman and
Seifu, 1989; Huffman et al., 1997; Wrangham, 1995), and a subsequent positivechange in this condition following ingestion(Huffman et al., 1993, 1996b).
The amount of detailed information on
self-medication gathered thus far is greatest
for the African great apes; however, selfmedication is expected to occur in othernon-human primates and other mammalian
species. The purpose of this paper is toreview the current range of evidence forpossible indirect and direct self-medicationin the African great apes and other nonhuman primates. Suggestive evidence ofsimilar self-medicative behaviors in othermammalian species will be discussed tounderline the important adaptive signi• cance of these behaviors. Finally, basic guide-̶ 262 ̶

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EVIDENCE FOR SELF-MEDICATION

lines for future research, predictions for the
future and practical application of thisknowledge will be discussed.
FOOD AS MEDICINE173

TABLE 1. Some common plant secondary compounds
and their effects on animals

Class of compounds

Effects (comments)

Terpenoid alkaloids

The gap between ‘medicine’ and ‘food’ inprimates may often seem transparent. Muchof what is consumed no doubt contains anarray of secondary compound(s). However,Johns (1990) argues that the herbal medicines and modern pharmaceuticals used byhumans today have replaced the non-nutritive chemicals commonly present in animal
diets. In this light, the non-nutritive components of a number of items ingested by
African great apes are worth mentioning
here. Their possible medicinal contribution
has received little attention in the past.
Secondary compounds
in fruits and leaves
Secondary compounds as well as inorganic materials are usually considered to bea plant’s front line defense against all but
the most specialized herbivores (Ehrlich andRaven, 1964; Feeny, 1976; Howe and Westley, 1988). These products are directly toxic
to the consumer or deter consumption by
reducing palatability or digestibility (Howeand Westly, 1988; Wink et al., 1993), yet anumber of items under this category can befound in the great ape diet.
The berries of Phytolacca dodecandra L
Herit (Phytolaccaceae) are an abundant andfrequently ingested food item of the
Kanyawara group in Kibale (Wrangham andIsabirye-Basuta, in Huffman and Wrangham, 1994). These bitter tasting berries area concentrated source of at least four toxic
triterpenoid saponins (lemmatoxin, lemmatoxin-C, oleanoglycotoxin-A, phytolacca-dodecandra glycoside), and ingestion of about
2 g of them by mice and rats is fatal. Foundin the highest concentration in the berry,these compounds are now being developedin the United States to control the level ofschistosome carrying snails (Abbiw, 1990;
Kloos and McCullough, 1987). Other known
properties of these triterpinoid saponins include antiviral, antibacterial, antifertility,
spermicidal and embryotoxic activities (Kloos
and McCullough, 1987). See Table 1 forother effects of common plant secondary
compounds.

Modulation of ion channels(highly toxic)
Isoquinoline alkaloids DNA intercalation, interaction
with receptors, causes
spasms (toxic and bitter)
Quinolizidine alkaloids Binding to ACH receptor (toxic
and bitter)
Tropane alkaloids
Inhibition of ACH receptor(highly toxic)
Pyrrolizidine alkaloids Mutagenic & carcinogenic(liver toxic)
Cyanogenic glycosides Inhibition of respiration
Cardiac glycosides
Inhibition of Na�/K�-ATPase(highly toxic)
Terpenes
Diuretic (bitter taste)
Volatile terpenes
Antibiotic, irritant
Volatile monoterpenes Antibiotic (aromatic smell)
Saponines, amines
Detergent for biomembranes(bitter)
Triterpene saponines
Detergent for biomembranes(toxic, emetic)
Sesquiterpenes, pyrPA are mutagenic & carcinorolizidines
genic, irritant (cytotoxic,
liver toxic)
Convallatoxin
Inhibition of Na�/K�-ATPase(highly toxic and bitter)
Anthraquinones
Purgative (toxic)
Phenolics
Astringency, reduces digestibility
Cellulose, hemicelluUndigestible
lose, lignins, silica

Prepared after Wink et al., 1993; Howe and Westley, 1988.

Pith and fruit of Afromomum species (wildginger family) are commonly ingested bychimpanzees, bonobos and gorillas across
Africa (cf. Idani et al., 1994; Moutsamboté etal., 1994; Nishida and Uehara, 1983; Sugiyama and Koman, 1992; Tutin et al., 1994;
Wrangham, 1977; Wrangham et al., 1993;
Yumoto et al., 1994). A study in progress ofthe chemical ecology of Bwindi gorilla (Gorilla gorilla beringei?; see Sarmiento et al.,1996) diet by John Berry (Rodriquez Laboratory, Division of Biological Sciences, Cornell
University) is investigating the bioactivityof the fruit of one of these wild ginger species, Afromomum sanguineum (K. Schum.)K. Schum. (Zingiberaceae). The fruits of thisspecies, in particular, are also known to beingested by gorillas at Kahuzi-Biega (Yumoto et al., 1994). Assays of homogenized
fruit and seed extracts show signi• ca nt antimicrobial activity (Berry, in preparation).
The fruits are sold locally in market stalls
and along the road in the Bwindi area for thetreatment of bacterial and fungal infection
and as an anthelmintic (Berry, personalcommunication).

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YEARBOOK OF PHYSICAL ANTHROPOLOGY

The tips of the young leaves of Thomandersia laurifolia (T. Anders. ex Benth.) Baill.
(Acanthaceae) are on rare occasion chewed
by western lowland gorillas (G. g. gorilla) in
the Ndoki forest of northern Congo (Kuroda,
Mokumu, Nishihara, in preparation). According to Kuroda and colleagues, the local human inhabitants use these leaves as a treatment for parasites and fever. Weakantischistosomal activity has also been foundfrom crude leaf extracts (Ohigashi, 1995).
Nutrient-poor bark and wood
Bark and wood are characteristicallyhighly • b rous, heavily ligni• ed, sometimes
toxic, relatively indigestible and nutrient
poor (Waterman, 1984). Chimpanzees andgorillas are known to infrequently ingest thebark and wood of several plant species (e.g.
Huffman and Wrangham, 1994).
While the list of plant species whose barkis ingested is long, little is actually known
about the contribution of bark to the dietand general health. The literature on African ethnomedicine warrants mention of afew of these species. The bark of Pycnanthus
angolensis (Welw.) Warb. (Myristicaceae) ingested by chimpanzees at Mahale is used byWest Africans as a purgative, laxative, digestive tonic, emetic and reliever of toothaches(Abbiw, 1990). Bark strips of Grewia platyclada K. Schum (Tiliaceae) are sometimes
chewed for the relief of stomach aches by
local residents at Mahale (Huffman, unpublished data, MS Kalunde, personal communication about human uses). In 1992 one juvenile male suffering from diarrhea wasobserved chewing and swallowing, but notingesting • b ers, of the bark of this species at
Mahale (Huffman, unpublished data).
Gombe chimpanzees occasionally eat thebark of Entada abyssinica Steud. ex A. Rich.
(Mimosaceae). In Ghana, the bark is used
for diarrhea and as an emetic (Abbiw, 1990).
The bark of Erythrina abyssinica DC. (Papilionacea) is occasionally eaten by Mahale
chimpanzees. Signi• cant plasmodicidal andantischistosomal activities have been demonstrated from the bark of this species collected at Mahale (Ohigashi, 1995; Wright etal., 1993). The bark of Gongronema latifolium Benth. (Asclepiadaceae) occasionallyeaten by Bossou chimpanzees is extremely
bitter, and the stems are used in West Africa[Vol. 40, 1997

as a purge for colic, stomach pains andsymptoms connected with intestinal parasite infection (Burkill, 1985).
The preceeding accounts of the ingestionof peculiar fruit, leaf, bark, and wood items
serve to demonstrate the diversity of secondary compounds or inferred pharmacologicalactivity present in great ape diets. It is also
possible that some of these examples, like T.
laurifolia, are indeed new cases of selfmedication, but have remained obscure forlack of detailed behavioral and health related data. The total effect of ingesting these
items is not clear, but it is too early toassume only nutritional gain.
Geophagy
Clay contains none of the essential components of nutrition; protein, carbohydrates,
lipids, and vitamins. Clay soils are • n egrained mineral deposits consisting mainlyof the hydrous silicates of aluminum magnesium and or iron. The chief groups of clay
minerals are kaolinite, halloysite, illite,
montmorillonite, and vermiculie whose outstanding property is the capacity for holding
water.
Geophagy is commonly practiced by many
animal species and humans world-wide (e.g.,
Halstead, 1968; Johns, 1990; Kreulen andJager, 1984). From the ethnographic literature, clay is consumed for its effectiveness as
an anti-diarrheal and is useful for the elimination of bitter taste, prevention of stomach
aches or vomiting after the consumption oflarge quantities of ‘famine foods’ high insecondary compounds (Johns, 1990). In nonhuman primates it has been described similarly as functioning to absorb tannins andother toxins acquired from a diet rich insecondary compounds (Davies and Baillie,
1988; Hladik, 1977a,b; Müller et al., 1997;
Oates, 1978). Overconsumption of clay however can lead to serious nutritional de• ciencies and illness (cf. Halstead, 1968; Kreulen,1985).
William Mahaney and colleagues associated with the Geophagy Research Project at
York University (Toronto, Ontario) have begun extensive studies in Africa (Rwanda,
Uganda, Tanzania, Guinea), Asia (Sumatra,
Borneo, Japan) and the Americas (Puerto
Rico) to analyze soils ingested by primatesand cattle. Thus far, evidence from joint

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EVIDENCE FOR SELF-MEDICATION

175

TABLE 2. Habitat description of African great ape study sites with documented or suspected medicinal plant use

Location,site name1

Species2

Altituderange

Approximate
location

Eastern Africa
Tanzania
MahalePts

773–2,515 m

6°07�S/29°44�E

Gombe

Pts

773–1,500 m

4°40�S/29°38�E

UgandaBwindiGg?

1,160–2,600 m

1°S/20°35�E

KibalePts

1,390–1,625 m

0°34�N/30°22�E

BudongoPts

1,050–1,200 m

1°45�N/31°20�E

Pts, Ggg

600–3,308 m

Pp

Zaire
Kahuzi-Biega
Central Africa
Zaire
Wamba
Congo
Ndoki

Vegetation type

Deciduous, evergreen gallery
forest, Miombo woodland
Deciduous dry and evergreen riverine forest, Miombo woodland,grassland

Averageannualrainfall

1,836 mm1,600 mm

Moist lower to upper montain
forest, bamboo, alpine on a gradientMedium altitude moist evergreen
forest, forest-grassland, swamp
Secondary mixed forest, swamp
forest, wooded grassland; selective logging

1,440 mm

2°S/28°E

Primary, secondary, swamp forest,
bamboo, sub-alpine

1,800 mm

370–430 m

00°11�N/22°28�E

Rainforest-derived mosaic of dry
swamp, secondary forest

2,000 mm

Ptt, Ggg

300–400 m

2°25�N/16°35�E

Seasonal rain forest, semi-deciduous, evergreen, swamp
forest, swamp clearing

1,540 mm

1,671 mm1,600 mmWestern Africa
Ivory CoastTai
GuineaBossouPtv

160–245 m

5°52�N/7°20�W

Evergreen moist forest

1,829 mmPtv

500–700 m

7°39�N/8°30�W

2,500 mm

Nimba

Ptv

400–1,752 m

7°32�N/8°28�W

Primary and secondary forest,
savana, cultivation
Primary forest, cultivation?

1 Source: McGrew et al., 1996, all sites except for Synnott, 1985 (Budongo); Sayer et al. 1992; Sarmiento et al., 1996 (Bwindi).
2 Pts: Pan troglodytes schweinfurthii; Ptv: P.t. verus; Pp: Pan paniscus; Gg?: Gorilla gorilla ?; Ggg: G.g. graueri.

geochemical and behavioral ecology studiesof the mountain gorilla and rhesus monkey
suggests that they may ingest soil for rareminerals of possible nutritional value or torelieve diarrhea caused by dietary changes(Mahaney et al., 1990, 1995a,b, 1996, 1997).
All clay soils analyzed thus far have beenshown to have components closely resembling those of Kaopectate, a pharmaceuticalcommercially sold to treat gastrointestinal
upset and other intestinal ailments (Mahaney et al., 1990, 1995a,b, 1996, 1997).
SELF-MEDICATIVE BEHAVIOR TYPES
Among the African great apes, one or bothof two proposed types of self-medicative
behaviors, bitter pith chewing and leaf swallowing, have been documented from 10 sites(Table 2; Fig. 1). The majority of the details
discussed below for these behaviors comefrom three study sites, Mahale (M group,
now extinct K group), Gombe (Kasakela,

now extinct Kahama), and Kibale (Kanywara, Ngogo). However, the geographical,
ecological and climatic variation of thesesites listed in Table 2 is great, ranging fromlower moist tropical forest and woodland tomontane forest located across the entire
distribution of the great apes in Africa. The
great variation in geography, ecology andclimate where leaf-swallowing and bitter
pith chewing is known to occur suggests thepossibility of their wider occurrence elsewhere. The known distribution of bitter pithchewing and leaf swallowing and geophagy
within the habitat of great apes is predicted
to grow as more attention is paid to them inthe future.
Bitter pith chewing
Hypothesis. Bitter pith chewing is currently proposed to aid in the control ofintestinal nematode infection, via pharmaco-

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YEARBOOK OF PHYSICAL ANTHROPOLOGY

176

Fig. 1.

[Vol. 40, 1997

African ape study sites with documented or suspected self-medication.

logical action, and relief from gastrointestinal upset. A description of bitter pith chewing and evidence for and against thishypothesis is discussed.
Behavioral ecology. The hypothesis that
bitter pith chewing has medicinal value forchimpanzees was • rs t proposed from detailed behavioral observations, and parasitological and phytochemical analyses of patently ill chimpanzees’ ingesting Vernonia
amygdalina Del. (Compositae) at Mahale(Huffman and Seifu, 1989; Huffman et al.,1993). These are the • rs t reported observations to verify illness and apparent improvement thereafter of an animal ingesting putative medicinal plants. Bitter pith chewing ofother Vernonia species has been observed atGombe (V. colorata (Willde.) Drake: Wrangham, 1975; Hilali, unpublished data as personal communication from J. Wallis) andKahuzi-Biega (V. hochstetteri Schi-Bip., V.
kirungae Rob. E. Fries: Yumoto et al., 1994;
A.K. Basabose, personal communication). At
Tai, the bitter piths of Paliosota hirsuta(Thunb.) K. Schum. (Commelinacea) andEremospath macrocarpa (Mann & Wendl.)
Wendl. (Palmae) are chewed (C. Boesch,personal communication). However, no details are available about the state of healthof individuals observed ingesting these species (Table 2).
V. amygdalina occurs throughout tropicalsub-Saharan Africa from as far north as
Ethiopia, Sudan, Guinea and Mali down toZimbabwe and Angola in the south (Burkill,
1985; Dalziel, 1937; Watt and Breyer-Brandwijk, 1962). Within the home range of M
group, this species is neither abundant nor
evenly distributed and usually occurs singly
along or near streams. Use by chimpanzeesof this plant often requires a detour from thegroup’s travel route. When ingesting thepith from young shoots of V. amygdalina,
chimpanzees meticulously remove the outerbark and leaves to chew on the exposed pith,from which they extract the extremely bitter
juice and residual amounts of • b er (Fig. 2).
The amount of pith ingested in a single boutis relatively small, ranging from portions of
5 to 120 cm � 1 cm (mean 54.57 cm, SD
41.01, n � 7). The entire process, dependingon the amount ingested, takes anywherefrom less than 1 to 8 minutes (mean 2.9
minutes, SD 2.59, n � 16, Uehara, Huffman, unpublished data). Mature conspecifics in proximity to an individual chewing
Vernonia bitter pith or leaf swallowing show
no interest in ingesting the pith (Huffman

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EVIDENCE FOR SELF-MEDICATION

Fig. 2. Bitter pith chewing of Vernonia amygdalina (top) and leaf swallowing (bottom) of Aspilia
mossambicensis.

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178

YEARBOOK OF PHYSICAL ANTHROPOLOGYand Seifu, 1989; Huffman et al., 1997). Infants of ill mothers, however, have been
observed on occasion to taste the pith discarded by their ill mothers. In one instance,
an appearently healthy mother prevented
her infant son from picking up a piece ofVernonia pith discarded by an adult male
who had just left. When the infant went over
to investigate, his mother put her foot on thepith and carried him away from it.
The ingestion of leaves or bark, the mostabundant parts of the plant available for
consumption by chimpanzees, is extremely
rare. Since 1965, ingestion of bark or leaves
have been observed one and two times respectively in K group (Uehara, personalcommunications) and leaves, but no bark,
only once in M group since 1968. Interestingly, the observation of V. amygdalina leaf
ingestion in M group in 1993 was by apatently ill adult male chimpanzee namedMusa, from a small tree that lacked any
usable fresh pith (Huffman et al., 1997,
1996b; unpublished data).
At Mahale, use of V. amygdalina has beenrecorded in all months except June andOctober (late dry season), demonstrating its
year-round availability (Nishida and Uehara, 1983). Despite year round availability,
use by chimpanzees is highly seasonal andrare. All but two of the eight cases of bitter
pith chewing recorded between 1971 and1974 occurred during the rainy season
months (November and May) (Nishida andNyundo, unpublished data). Bitter pithchewing was directly observed seven times
in M group between 1985 and 1997 during a
total of 728 hours of focal observation i.e.,
one feeding bout per 104 hours (Huffman,
unpublished data). All of these cases occurred between November and February.
Data collected on the 30 member K group
continuously over a 24 month period between 1976 and 1978, shows a statisticallysigni• ca nt tendency for the more frequent
occurrence of bitter pith chewing during therainy season (n � 36/38 days occurred inrainy season, z � 67.41, P � 0.0001;
weighted for differential length in seasons;in Huffman et al., 1990). A peak in thefrequency of bitter pith chewing was noted
during December-January just after the onset of the rainy season (data not shown).

[Vol. 40, 1997

Interannual variation does occur. Despite
plant availability, in some years bitter pithchewing is not observed. This suggests thatfactors other than plant abundance in• uence the frequency of occurrence of thisbehavior.
Parasite infection and general health.
A longitudinal investigation of the intestinal
parasite fauna of Mahale chimpanzees showsthat they are infected by three parasite
species from three genera of nematode,
Strongyloides fulleborni (thread worm),
Trichuris trichiura (whip worm), and Oesophagostomum stephanostomum (noduleworm); one genus of trematode, Dicrocelium
lanceatum (lancet • uke); and four genera of
protozoa, Entamoeba coli (amoeba), Endolimax nana (amoeba), Iodamoeba buetschlii(amoeba), and Giardia lamblia (amoeba
which causes giardiasis) (Huffman et al.,1997). Chimpanzees were monitored individually over time to detect weekly, monthly,and yearly changes in infection levels. Among
all M group chimpanzees monitored in 1991–
1992 and 1993–1994, a statistically signi• cant rainy season increase in the incidence
of infection was noted only for individuals
infected by nodular worms (Fisher’s exact
test, P � 0.0001, P � 0.01, respectively in
Huffman et al., 1997). Among all three nematode species detected, nodular worm (95%,
14/15) infections were associated signi• cantly more frequently with bitter pith chewing (n � 3) and leaf swallowing (n � 17)
during the same two study periods thaneither whip worms (50%, n � 7) or thread
worms (40%, n � 6) (Fisher’s exact test for
O.s.-T.t., P � 0.0142; O.s.-S.f., P � 0.005 in
Huffman et al., 1997).
General observations on the state of healthat the time bitter pith was chewed wereavailable for four of the 10 cases recorded
between 1987 and 1996 in M group. In all
four cases, ill health was evidenced by thepresence of diarrhea, malaise and nematodeinfection (Huffman et al., 1997). Detailed
observations were available from longer focal observations in two of these cases. Recovery within 20–24 hours from a lack of appetite, malaise, and constipation or diarrhea
was recognized (Huffman and Seifu, 1989;
Huffman et al., 1993). In one case the eggs

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EVIDENCE FOR SELF-MEDICATION

179

TABLE 3. Plant species whose bitter piths are ingested by African great apes

Eastern Africa
Tanzania
Mahale(Pts)

Family, species
Compositae
Vernonia amygdalina Del.
V. colorata (Willde.) Drake
V. hochstetteri Schi-Bip.
V. kirungae Rob. E. Fries
Commelinacea
Palisota hirsuta (Thunb.) K. Schum.
PalmaeEremospatha macrocarpa (Mann & Wendl.) Wendl.

Gombe
(Pts)

Western Africa
UgandaIvory Coast

Kahuzi-Biega(Pts, Ggg)

Tai
(Ptv)

X
X
X, X
X, X
X
X

Reference of plant use data: Mahale, Huffman and Seifu, 1989; Gombe, Huffman and Wrangham, 1994; Kahuzi-Biega, Yumoto et al.,
1994; A.K. Basabose, personal communication; Tai, C. Boesch, personal communication.
Pts, Pan troglodytes schweinfurthii; Ptv, P.t. verus; Ggg, Gorilla gorilla graueri?

per gram feces (EPG) level of a nodular
worm infection could be measured and wasfound to have dropped from an EPG count of
130 to 15 within 20 hours. No change occurred in this individual’s concurrent whip
worm infection (Huffman et al., 1993). When
compared to seven other individuals withnodular worm infections monitored over thesame period, this was the only case in whichsuch a dramatic drop in EPG was noted for
nodular worm infections. A decrease was
detected in only two of seven other individuals monitored over the same period. In one
case the drop was minimal (15 EPGs). In theother case a total drop of 510 EPGs over 18days was noted. Unfortunately, the patently
ill male was absent from the group for mostof this time and when he could be followed,
use of V. amygdalina was not observed. It
was impossible to determine whether herecovered on his own or attempted someform of self-medication. In the remainingcases, nodular worm EPG levels increased
over time. The average increase was 69.9
EPG (SD � 84, range 5–236). The upper
EPG • gu res of this range are biased by theextended time period of several weeks in
between counts. The recognized increases in
EPG levels represent the overall trend forincreased reinfection by nodular worms at
the beginning of the rainy season (Huffman
et al., 1997).
O. stephanostomum is the most hazardous
species of nodular worm found in the great
apes (Brack, 1987). Repeated infection, as is
expected to occur in the wild, causes signi• cant complications including secondary bacterial infection, diarrhea, severe abdominal

pain, weight loss, and weakness resulting inhigh mortality (Brack, 1987). Whip worm
and thread worm infections usually are notserious and may go unnoticed in mild tomoderate cases (Brach, 1987). The serious
effects of nodular worms on the host, however, suggests that it may be an important
stimulus for bitter pith chewing and otherantiparasite behaviors.
Ethnomedicinal and phytochemical evidence. For numerous African ethnic
groups, a concoction made from V. amygdalina is prescribed treatment for malarial
fever, schistosomiasis, amoebic dysentery,several other intestinal parasites and stomachaches (Burkill, 1985; Dalziel, 1937; Huffman et al., 1996a; Watt and Breyer-Brandwijk, 1962).
Some of the species with bitter piths ingested by chimpanzees at Gombe, KahuziBiega, and Tai (Table 3) also have a numberof ethnomedicinal and pharmacological properties worth mentioning. V. colorata and V.
amygdalina, very closely related species,
are not distinguished from each other bytraditional African healers with regard totheir medicinal properties and folk classi• cation (Burkill, 1985). Alkaloids occur in thepith, as well as • ow er and leaf of V. hochstetteri (Smolenski et al., 1974). P. hirsuta andE. macrocarpa are used in west African
ethnomedicine for the treatment of upset
stomachs, colic, as an antiseptic and analgesic and for venereal disease (Abbiw, 1990;
Neuwinger, 1996). Moluscicidal activity has
also been reported for P. hirsuta (Okunji andIwu, 1988).

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YEARBOOK OF PHYSICAL ANTHROPOLOGY[Vol. 40, 1997

Fig. 3. Chemical structures of the steroid glucosides and sesquiterpene lactones isolated from
Vernonia amygdalina.

The noted recovery time of 20–24 hours
after bitter-pith chewing in two M groupchimpanzees is comparable to that of local
human inhabitants, the Tongwe, who use
cold concoctions of this plant as a treatment
for parasites, diarrhea and stomach upset.
These observations encouraged Huffman andcolleagues to investigate the possible contribution of plant secondary compounds in V.
amygdalina against parasite infection. Phytochemical analysis of V. amygdalina
samples collected at Mahale in 1989 and1991 from plants known to be used bychimpanzees revealed the presence of two
major classes of bioactive compounds (Fig.
3). From this work to date, a total of four
known sesquiterpene lactones (vernodalin,vernolide, hydroxyvernolide, vernodalol),
seven new stigmastane-type steroid gluco-

sides (vernonioside A1–A4, B1–B3) and two
freely occurring aglycones of these glucosides (vernoniol A1, B1) have been isolated(Ohigashi et al., 1991; Jisaka et al., 1992a,b,
1993a,b). Figure 3 shows the newly determined chemical structures of the steroid
glucosides and the widely known sesquiterpene lactones found so far in V. amygdalina.
Supportive of the ethnomedicinal literature, the sesquiterpene lactones present in
V. amygdalina, also found in V. colorata anda number of other Vernonia spp., are wellknown for their anthelmintic, antiamoebic,
antitumor, and antibiotic properties (Asakaet al., 1977; Gasquet et al., 1985; Jisaka etal., 1992a, 1993b; Kupchan et al., 1969;
Toubiana and Gaudemer, 1967). From crude
methanol extracts of the leaves, Koshimizu
et al. (1993) also found inhibition of tumor

̶ 270 ̶

Huffman]

EVIDENCE FOR SELF-MEDICATION

promotion and immunosuppressive activities.
In vitro tests on the antischistosomal activity of the pith’s most abundant steroid glucoside (vernonioside B1) and sesquiterpene
lactone (vernodaline) showed signi• cant inhibition of movement of the adult parasites
and adult females’ egg-laying capacity(Jisaka et al., 1992b). These • nd ings are
consistent with the observed decline in nodular worm EPG level 20 hours after an adultfemale chimpanzee at Mahale ingested V.
amygdalina pith (Huffman et al., 1993).
At 200 ppm, vernonioside B1 signi• cantly
inhibited both movement and egg-laying. At
20 ppm, however, the effects of B1’s primary(vernoniol B1) and secondary aglycones weremore active than vernonioside B1 itself, especially against the movement of schistosomes. Similarly, the inhibition of movement activity of A4’s aglycone vernoniol A4
was remarkably higher than that of vernonioside A4 itself (Ohigashi et al., 1994).
While these aglycones are naturally present
within the pith, they are not as abundant as
either vernonioside B1 and A4 (Jisaka et al.,1992a). However, their concentrations arethought to increase as B1 or A4 are metabolized into these more effective forms byhydrolysis after ingestion (Jisaka et al.,1992a; Ohigashi et al., 1994).
In vivo tests of the most active antischistosomal constituent vernodalin proved lethal
to schostosome cercaria-infected mice whenorally administered at 5 mg per mouse, andinjected abdominally at 2 mg, or subcutaneously or intramuscularly at 5 mg, per mouse(Jisaka et al., 1992b). While abundant in theleaves and bark, this highly toxic compoundoccurs in only insigni• cant amounts in thepith. This would explain why chimpanzees
normally avoid ingesting leaves and bark in
preference for the pith, with its greater
abundance of steroid glucosides and perhaps their aglycones (Jisaka et al., 1992a;
Ohigashi et al., 1994).
In vitro tests on the antiparasitic activityof both the sesquiterpene lactones and thesteroid glucosides using Leishmania infantum (produces visceral leishmaniasis), Entamoeba histolytica (produces amoebic dysentery), and a K1 multi-drug resistant strainof Plasmodium falciparum (produces falcipa-181

rum malaria) have also been conducted (Ohigashi et al., 1994). The sesquiterpene lactones showed signi• cant plasmodicidal
activity although the IC50 values were morethan 20 times higher than that of the common commercial agent, chloroquine diphosphate (Ohigashi et al., 1994). The steroid
glucosides showed weaker plasmodicidal activity. However, as in the case describedabove, the activity of their aglycones was
signi• cantly higher in both plasmodicidal
and amoebicidal testing. In particular, asigni• cant increase in the plasmodicidal activity of vernoniol A4 was noted (Ohigashi etal., 1994).
The evidence described above from parasitological, pharmacological and ethnomedicinal observations is substantial and lends
support to the hypothesis that bitter pithchewing is stimulated by, and controls nematode infection. The direct evidence demonstrating a signi• ca nt drop in nodule worm
infection or marked improvement in healthafter use, however, comes from only two
detailed case studies in the • eld . All cases
obtained since then from direct observation
have veri• ed illness at the time of use, but
sufficient data to reliably support or reject
recovery could not be obtained. Due to therarity of this behavior it has been extremely
difficult to increase the number of cases forcritical evaluation. It will be necessary to
conduct controlled in vivo studies in the
future on compatible animals models inorder to reliably test this hypothesis further.
Plans are now underway to do so (see below).
Leaf swallowing
Hypotheses. Leaf swallowing is currently
proposed to control strongyle nematode infection and relieve pain caused by tapeworm
infection by expelling these intestinal parasites. Both phytochemical and physicalmechanisms for parasite removal have been
proposed. A description of leaf swallowing
behavior and evidence for and against thesealternative hypotheses are discussed.
Behavioral ecology. Leaf swallowing behavior in the great apes was • rst recorded
for chimpanzees at Gombe and Mahale(Wrangham, 1977; Wrangham and Nishida,1983). It came to the attention of observers

̶ 271 ̶

182

YEARBOOK OF PHYSICAL ANTHROPOLOGY

at both sites that leaf swallowing was unlikely to provided any nutritional value after
they found the folded, undigested leaves of
Aspilia mossambicensis (Oliv.) (Compositae), A. pluriseta (O. Hoffm.) Wild, and A.
rudis Oliv. & Hiern in the dung. The puzzling manner of ingesting Aspilia spp. andthe suggestion that chimpanzees may possess a sophisticated pharmacopoeia (Rodriguez et al., 1985) drew the attention ofother • el d researchers to look for similar
anomalous feeding habits among apes intheir study sites (e.g., Boesch, 1995; Huffman, 1993; Matsuzawa and Yamakoshi,
1996; Sugiyama and Koman, 1992; Takasaki
and Hunt, 1987). As of January 1, 1997, leaf
swallowing behavior involving 30 different
plant species has now been observed in nine
populations of chimpanzee (Pan troglodytes
schweinfurthii, P.t. troglodytes P.t. verus)
and in one each of bonobo (P. paniscus) andeastern lowland gorilla (Gorilla gorilla
graueri) populations at 10 sites across Africa(Table 4; Fig. 1). The plant species used varyin life form (herb, vine, shrub, tree), but thecommon property linking all of these plants
is their hairy and rough-surfaced leaves. As
shown in Figure 4 from SEM photographs ofthe leaf surface of • ve representative species, trichome structure varies from longand slender (A, C, D), thorn like (B), hooked(C, not shown here but hooked hairs are aparticular characteristic of A. aequinoctiale), and spiked (E).
The distal half of these leaves are selected
one at a time, folded by tongue and palate as
they are slowly pulled into the mouth andthen individually swallowed whole (Fig. 2).
The leaves’ roughness no doubt makes themdifficult to swallow, so folding them with the
tongue and palate before swallowing is considered to be a necessary part of ingestion.
An individual may swallow anywhere from
one to 100 leaves in one bout, at a medianrate of • ve leaves per minute (range 2.4–
15.4 min., n � 7 bouts; data from Wrangham and Goodall, 1989). An individual may
visit more than one bush in a day (Huffman
et al., 1996b; Wrangham and Nishida, 1985).
Chimpanzees at Gombe, Mahale, Kibale
and Tai are reported to swallow leaves, withclear exceptions at Mahale, early in the[Vol. 40, 1997

morning or within the • rst few hours after
leaving their sleeping nests (Boesch, 1995;
Wrangham and Goodall, 1989; Wrangham
and Nishida, 1983; Huffman et al., 1996b)
and thus, on a relatively empty stomach.
The leaves of at least four species reported tobe swallowed by apes in Table 4 (A. mossambicensis, Trema orientalis (L) Blume syn. T.
quineensis (Ulmacea), Ficus exasperata Vahl,
and F. mucuso Fichalho (Moraceae)) are also
chewed when ingested by chimpanzees atother times (Nishida, Huffman: Mahale; Yamakoshi, Takemoto: Bossou, unpublisheddata). F. exasperata in particular is also acommon food source by chimpanzees andother non-human primates at these andother study sites. This habit of chewing toingest large amounts of the same leaf material swallowed without chewing at othertimes presents an intriguing dichotomy ofuse.
Longitudinal data on the temporal occurrence of leaf swallowing taken from both
direct observations and the presence ofleaves in the dung are available currently
only for Aspilia sp. at Mahale (K group) and
Gombe (Kasakela, Kahama communities),and for A. aequinoctiale (P. Beauve) Loudon(Commelinaceae) and R. cordifolia L (Rubiaceae) at Kibale (Kanyawara, Ngogo). At allof these sites, leaf swallowing is an extremely rare behavior. An average rate ofonce per every 69.0 hours (n � 18 bouts
during 1,242 hours) and once every 81.9
hours (n � 11 bouts during 901.37 hours) for
A. mossambicensis at Mahale and once per
every 102.6 hours (n � 10 bouts during 1,026
hours) for Aspilia spp. at Gombe have beenreported (Wrangham and Nishida, 1983; S.
Uehara, unpublished data).
Aspilia leaves are available year-round at
both Gombe and Mahale. Direct observationand the inspection of dung for the presenceof whole leaves con• rm s this by showingthat Aspilia spp. leaf swallowing has occurred in all months except April and November at Gombe, and every month at Mahale(Wrangham and Goodall, 1989; Wrangham
and Nishida, 1983). Nonetheless, interannual variation in the frequency of leaf swallowing at Mahale and Gombe is substantial.
At Mahale use was most common after the
beginning of the rainy season (November–̶ 272 ̶̶ 273 ̶
10

X

X

X

X
X

X
X

X

X

X

3

X

X
X

Gombe
(Pts)

3

X

X

X

3

X
(1 sp.)

X
X

Budongo(Pts)

UgandaKibale
(Pts)

5

X
X
X

X

X, X

Kahuzi-Biega(Ggg, Pts)

Zaire

1

X

Wamba
(Pp)

Central Africa

1

X

Ndoki
(Ptt)

Congo

6

X
X
X
(2 spp.)

X
X

Tai
(Ptv)

1

X

Nimba
(Ptv)

Ivory Coast

6

X

X

X

X
X
X

Bossou(Ptv)

GuineaWestern Africa

Source of plant use: Mahale, Huffman, 1993, Huffman et al., 1996b, 1997, Huffman and Wrangham, 1994, T. Nishidsa, H. Takasaki, M. Hamai, personal communication; Gombe, Wrangham and Nishida,
1983, Wrangham and Goodall, 1989; Kibale: Wrangham, 1995; Budongo, C. Bakuneeta, V. Reynolds, personal communication; Kahuzi-Biega, Yumoto et al., 1994, A.K. Basabose, J. Yamgiwa, personalcommunication; Wamba: S. Kuroda, personal communication; Ndoki: S. Kuroda, T. Nishihara, personal communication; Tai: C. Boesch, 1995 and personal communication; Nimba: Matsuzawa andYamakoshi, 1996; Bossou: G. Yamakoshi, H. Takemoto, personal communication.
Pts, Pan troglodytes schweinfurthii; Ptt, P.t. troglodytes; Ptv, P.t. verus; Pp, P. paniscus; Ggg, Gorilla gorilla graueri.

n � 30 spp. (incl. 3 unidenti• ed spp.)

Compositae
Aspilia mossambicensis (Oliv.)
A. pluriseta (O. Hoffm.) Wild
A. rudis Oliv. and Hiern
Malvaceae
Hibiscus aponeurus Sprague and Hutch
Verbenaceae
Lippia plicata Baker
Commelinaceae
Commelina diffusa Burm. f.
C. benghalensis Linn.
C. cecilae C.B. Clarke
Aneilema aequinoctiale (P. Beauv.) Loudon
A. nyasense C.B. Clarke
Rubiaceae
Rubia cordifolia L.
Gramineae
Hyparrhenia cymbaria (Linn.) Stapf
Moraceae
Ficus exasperata Vahl
F. mucuso Ficalho
Antiaris africana Engl.
Ulmaceae
Trema orientalis (L) Blume syn. T. quineensis
Celtis ador• -frederici Engl.
Melastomataceae
Melastomastrum capitatum Vahl A. and R. Fernandes
Tristemma coronatum Benth.
Dichaetanthera africana (Hook. f.) Jac.-Fel. l.c. (syn. Sakersia africana)
Convolvulaceae
Ipomoea involucrata P. Beauv.
Cucurbitaceae
Lagenaria abyssinica (Hook. f.) C. Jeffrey
Adenopus abyssinicus Hook. F.
Peponium sp.
Icacinaceae
Polycephalium capitatum (Baill.)
Euphorbiaceae
Maniophyton fulvum Mull. Arg
Cyperaceae sp.
Unidenti• ed spp.

Family, species

Mahale(Pts)

Tanzania

Eastern Africa

TABLE 4. Plant species swallowed whole by African great apes

184

YEARBOOK OF PHYSICAL ANTHROPOLOGY[Vol. 40, 1997

Fig. 4. Electron micrographs of the upper leaf surface of • v e species swallowed whole by chimpanzees.
A: A. mossambicensis. B: L. plicata. C: A. aequinoctale. D: H. aponeurus. E: T. orientalis and the mouthpart of the intestinal nematode. F: O. stephanostomum (scale bar � 500 µm). From Huffman et al.
(1996b).

May) with peak frequencies in January andFebruary being 10–12 times higher thanthose of other months (Wrangham andNishida, 1983). Direct observations and dungsamples collected from the Mahale K groupover a continuous 24 month period, between
1976 and 1977, illustrate the tendency observed in other years for the more frequent
occurrence of leaf swallowing during therainy season. Leaf swallowing occurred on a
statistically signi• ca ntly greater number ofdays in the rainy season than in the dry
season (n � 19/20 days occurred in rainyseason, binomial test z � 67.41, P � 0.0003;
weighted for differential length in seasons;unpublished data by Uehara and Nishida in
Huffman et al., 1990). In Gombe peak frequencies of use were also observed in January (4 years), February (2), March and May(2), but also once in July (Wrangham andGoodall, 1989).
At Kibale, direct observations have been
made only three times, but systematic dungcollection from December 1987 to May 1994
provides evidence (n � 44) for leaf swallowing in both Kanywara and Ngogo chimpanzees (Wrangham, 1995). Leaves of A. aequinoctiale and R. cordifolia are swallowed byboth Kanyawara and Ngogo chimpanzees;
however, the leaves of both species were
found signi• ca ntly more often in the dung of
Kanyawara chimpanzees (A. aequinoctiale:
Wilcoxon z � 2.97, n � 13 with nontied datafrom both sites, P � 0.01; R. cordifolia:z � 2.27, n � 13, P � 0.05; Wrangham,
1995). Leaves were found in the dung of
Kanyawara chimpanzee in all months (78months) except September, November and̶ 274 ̶

Huffman]

EVIDENCE FOR SELF-MEDICATION

December, with repeated peaks in the periods between January–February, March,
April–June and July (calculated from Figure 1 of Wrangham, 1995). Unlike the distinct dry (June–October) and rainy (November–May) season pattern of Gombe andMahale, rainfalls more evenly throughout
the year at Kanyawara with two ‘‘wet periods’’ (approx. March–May and August–November) and two drier ‘‘transitional periods’’ (approx. December–February andJune–July) but no extended dry season(Struhsaker, 1997). Based on this generalcriteria, no signi• can t difference was detected in the frequency of leaf swallowing
between the wet and transitional periods at
Kanyawara (Mann-Whitney U-test, corrected for ties, z � �.917, P � 0.3594; percent of dung containing whole leaves/month
was estimated by the author to the nearest
whole number from Figure 1 of Wrangham,
1995).
Parasite infection and general health.
Information on parasite infection and healthat the time of leaf swallowing is only available from observations at Mahale and Kibale.
This information varies in a number ofimportant aspects so these two sites will be
discussed separately below.
Mahale. Behavioral pro• l es were collectedconcurrently with all cases of leaf swallowing observed during a 4-month study from
December 1993 to February 1994 at Mahale(Huffman et al., 1996b). As part of thisprocedure, dung samples were systematically inspected during focal-animal and ad
libitum observations. This was done to macroscopically check for the presence of whole
leaves and parasites in the dung, to monitor
general health by stool type (diarrheal or
normal) and to collect samples for microscopic evaluation of nematode infection levels, in the laboratory. Nematode infection
was demonstrated in 83% of all cases of leaf
swallowing documented (n � 10/12 cases, 11
individuals; • v e from dung samples; sevenfrom direct observation, Huffman et al.,1996b). Multiple species infections were common, but nodular worm infections (78%)
were most commonly associated with leaf
swallowing behavior; followed by those of185

thread worms (56%) and whip worms (33%).
Infection by other intestinal parasite species
were rare and inconsequential during thisstudy period. As noted above, during therainy season there is a signi• cant trend forthe increase in the number of individuals
infected with nodular worms at Mahale.
Thread worm infections remained low yearround and whip worm infections were inconsistent from year to year in their rainyseason–dry season prevalence of infection(Huffman et al., 1997). The presence of these
two nematode species may have intensi• ed
symptoms of illness, but alone their impact
on chimpanzees was not found to be substantial.
Symptoms which may be caused by infections from these nematodes (diarrhea, malaise, abdominal pain; Brack, 1987; Anderson, 1992) were veri• ed from direct
observation in seven of the eight chimpanzees at the time that leaves were swallowed(Huffman et al., 1996b, 1997). Parasite
worms, all later identi• ed as nodular worms(Oesophagostomum stephanostomum; body,ca. 2.5 cm), were found in 3.7% (n � 9/254) of
the dung collected from focal and non-focal
individuals. The occurrence of worms in thedung was rare and limited to individuals
that displayed symptoms of malaise anddiarrhea.
Kibale. Longitudinal microscopic data fornematode infection in Kibale chimpanzees
are not available. However, the most frequently occurring genera of parasites in
Kibale, Gombe, Mahale and Budongo chimpanzees have been reported to be a nodular
worm species (Oesophagostomum spp.) followed by thread worms and whip worms(Barrows, 1996; File et al., 1976; Huffman etal., 1997; Rodriguez and Wrangham, 1993).
During a 78-month monitoring period of chimpanzee dung between 1987 and 1994 at
Kanyawara, tapeworm proglottid fragments(Bertiella studeri) were found in 1% (16/
1,696) of the total chimpanzee dungs inspected. This occurrence of tapeworm fragments in the dung was restricted to a
6-month period (‘‘transitional-wet-transitional’’) referred to by Wrangham as theperiod of tapeworm infection. Note howeverthat the absence of tapeworm fragments in̶ 275 ̶186

YEARBOOK OF PHYSICAL ANTHROPOLOGY

the dung does not rule out the possibility of
tapeworm infection. Infection can be proceeded by as long as 2 years before proglottids of this species appear in the feces ofhumans (Beaver et al., 1984).
Direct observation of leaf swallowing at
Kibale has only been observed three times.
Parasite infection and a general evaluationof health around the time of leaf swallowing
could only be inferred from macroscopic
dung analysis (Wrangham, 1995). From 12dungs containing tapeworm fragments collected during this 6 month period, threewere diarrheal and another three werescored as intermediate between diarrheal
and normal. From this it was suggested thatsome chimpanzees egesting tapeworm fragments may experience digestive disturbances, but it was not mentioned if thesedungs contained leaves or not (Wrangham,
1995).
Parasites and the possible functions
and mechanisms of leaf swallowing
The Mahale nodular worm hypothesis. The
nematode control hypothesis derived from
the Mahale leaf swallowing data complements that of bitter pith chewing in function
but differs in its proposed mechanism. At
Mahale both behaviors are sometimes displayed by the same individual on the same
day and together may have a synergetic
affect on nodular worm infection. In 1993–
1994, six of the nine dungs (n � 254) foundto contain worms also contained whole undigested leaves of A. mossambicensis, T. orientalis or A. aequinoctiale. The remaining
three dungs containing worms but no leaves
were collected from three of the individuals
whose dung contained both leaves and worms
earlier that day (Huffman et al., 1996b).
This suggests that worms may continue tobe expelled for a short while after leaves
have been egested. In only one case were
worms not found in the dung when leaves
were present during the same study period.
The relationship between the presence ofboth leaves and nodular worms in the dung
was highly signi• ca nt (Fisher’s exact test,
two sided, P � 0.0001; Huffman et al.,1996b). From this it was observed that a[Vol. 40, 1997

strong relationship between leaf swallowing
and the expulsion of nodular worms existed.
A possible mechanism for nodular worm
expulsion was partially deduced from theexamination of three of these dung samples
which contained leaves and worms. The
contents of these dung were macroscopicallyinspected 4 days after collection, having
been stored in plastic bags and kept in a cooldark room. The contents of the dung were 18
leaves:18 worms, 51:21 and 1:2 respectively.
In one dung, two nodular worms were found• rm ly attached by the trichomes to thesurface of an A. aequinoctiale leaf as if by
Velcro. The majority of the other nodular
worms were trapped within the folded leaves.
All worms where alive and motile at thetime of inspection.
It is unlikely that the total number ofworms and leaves from one stool represents
the total outcome of one leaf swallowing
bout. Unfortunately it is impossible to verify
the total outcome of a leaf swallowing boutin the wild because not all dungs can becollected and not all cases of leaf swallowing
can be observed from an individual over theentire course of its illness. Leaf swallowing
appears to affect only nodular worms. Nodular worms inhabit the large intestine, where
they attach by the buccal capsule (Fig. 4).
This attachment is not permanent andworms move around the intestine in searchof food and mates (Anderson, 1992). Adult
thread worms (2 mm) and whip worms(30–40 mm) on the other hand are smaller
and burrow into the mucosa of the small
intestine and caecum, respectively, where
they embed themselves • rm ly (Anderson,1992) and thus are not considered to besusceptible to mechanical removal by theleaves. The ‘‘control of nematode infection
hypothesis’’ predicts that since nodular worm
infections are typically self-limiting (Beaver
et al., 1984), the total infection may becontrollable if a chimpanzee periodicallyswallows leaves during the most likely period of reinfection. In general, for all nodular
worm species the peak period of reinfectionis the rainy season (Krepel et al., 1995). At
Mahale the peak period of reinfection by the
nodular worm O. stephanostomum was foundto occur 1 to 2 months after the onset of therainy season around December or January̶ 276 ̶

Huffman]

EVIDENCE FOR SELF-MEDICATION(Huffman et al., 1997). This is also the time
when chimpanzees tend to swallow leaves(and chew bitter pith) most frequently at
Mahale and Gombe (Huffman et al., 1990,
1996b, 1997; Wrangham and Goodall, 1989;
Wrangham and Nishida, 1983). The continued expulsion of adult worms over time fromsuccessive bouts of leaf swallowing may bepartially responsible for the observed decline in total nodular worm egg burdens(directly correlated to the number of egg
laying adults) later on in the rainy season(Figure 2 in Huffman et al., 1997).
Nodular worms produce abdominal pain
along with bowel irritation and diarrhea(Brack, 1987), symptoms which could provide ample stimulus for leaf swallowing
behavior in chimpanzees infected with thisnematode (Huffman and Seifu, 1989; Huffman et al., 1993, 1996b).
The Kibale tapeworm hypothesis. In 1993,
signi• cantly more leaves (8.5% of 271 dungs)
were found in dungs during the 6-month
period of tapeworm fragment egestion thanin the dungs outside of this period (1.3% of
1,425 dung collected between 1987 and 1992)(Mann-Whitney z � 4.32, P � 0.001; Wrangham, 1995). Also, the proportion of dungs
with both tapeworm fragments and leaves(21.7% n � 23) was signi• cantly higher thanthe proportion of dungs with whole leaves
and no tapeworm fragments (3.6%, n � 248;
Binomial test, z � 4.46, P � 0.001; Wrangham, 1995). From this Wrangham concluded
that whole leaves in the gut increase theprobability of tapeworms fragments being
shed.
Whole leaves were found in dung during
21 months of the survey, while leaves andtapeworms were found together in only 33%of these months. It is possible that sometapeworm fragments went undetected. The
greater overall occurrence of leaves in dung
without tapeworms, however, suggests thatthe expulsion of proglottid fragments may
not be the direct function of leaf swallowing.
Wrangham (1995) proposes that the stimuli
for leaf swallowing as observed at Kibale
could be abdominal pain caused by tapeworm infections and thus leaf swallowing
may function to alleviate pain. In this light,
it seems likely that chimpanzees were re-187

sponding to discomfort from the presence of
tapeworms in the intestines before tapeworm proglottid fragments began to appear
in the dung. This would explain the long
period of leaf swallowing observed before
proglottid expulsion.
Comparative evidence for tapeworm expulsion and leaf swallowing. Observations of undigested plant leaf material andlarge masses of tapeworms in the dung of
Alaskan brown bears by Barrie Gilbert (Department of Fisheries and Wildlife, Utah
State University) suggest some striking similarities with African apes in both mechanism and function. Gilbert observed what
• rs t appeared to him as anomalous plant
ingestion in the fall months just prior tohibernation by Alaskan brown bears during
a 6-year behavioral study at Brooks River in
Katmai National Park, Alaska (B. Gilbert,
personal communication).
During the spring in coastal regions, abrown bear’s diet consists 100% of estuarine
sedge (Luque and Stokes, 1976). Carex sp.
(Cyperaceae) was the species ingested before salmon arrived. Note that an unidenti• ed species of Cyperaceae is also swallowed
whole by chimpanzees at Tai (Table 4). At
this time of year sedge consumption is highly
correlated with an increased phase of protein content and low structural cellulose. In
the fall, however, foraging is consistently onhigh fat-content items, de• nit ely eliminating sedge, which is rather inefficiently digested, even in its least woody phase of
growth in spring. In the fall, Carex sp. is
extremely high in • bre tissue, rather sharpedged and coarse. At this same time, large
dung masses, almost completely composedof long tapeworms, are often observed. The
tapeworms appeared to be expelled in nearentirety, although worms were never examined closely enough to see if the scolex waspresent.
These observations lead Gilbert to question what an animal would suffer in energy
loss, etc., if it went into hibernation for 6–7
months with a gut lined with tapeworms. He
presumes that, as the temperature of bears
is within a few degrees of normal duringhibernation, gut parasites would not become
particularly inactive. Bears eat prodigious

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YEARBOOK OF PHYSICAL ANTHROPOLOGY

quantities of decomposed salmon, making
their liquid feces rich in digestible nutrients.
With the hyperphagia of bears in fall and thevolume of liquid salmon in their guts, tapeworms would • ourish and thus be a distinct
liability during hibernation. However, parasite levels in hibernating bears are in fact
quite low (Choquette et al., 1969).
What Gilbert proposes is that the coarse
leaf material functions as a rasping plug or‘‘Brillo’’ pad to scrape off the scolices. In
effect, if a bear were to ingest coarse leaf
material prior to going into hibernation, thismight help to decrease its tapeworm load.
This mechanical action would account forthe observation of dung composed almost
completely of tapeworms. Previously, theloss of tapeworms each year before hibernating and reinfection in the spring has been
ascribed to a change in diet (Rausch, 1954,
1961). The above account suggests that themanner in which items of no nutritional
value are ingested is of critical importance.
John Holmes (Parasitology, Departmentof Biological Sciences, University of Alberta)
has noted a similar phenomena in Canadiansnow geese. In the summer prior to theirmigration south, juvenile birds in particular
carry signi• can t tapeworm burdens. Also at
this time of year, Holmes observed largeboluses of undigested grass and tapeworms
in goose dung. When the parasite loads ofthese same • ocks were measured after migrating south, their mid-lower guts were
found to be completely clean, with no scolices attached. In both of the cases mentioned
above, tapeworms were shed around a timeof critical nutritional stress. This too may
help to clean the gut of bacteria and parasites that may be a problem during long
periods of winter inactivity.
Feeding is greatly reduced or stopped
entirely when these animals are hibernating or migrating. During these critical periods the cost of competition with gut parasites for a limited source of metabolites andstored energy is expected to be high. Similar
purging may be applicable to ape populations, like Kibale, where tapeworm burdens
are prevalent. If so, it can be predicted thatthe relative frequency of leaf swallowing
would increase during periods of combined
food stress (e.g., fruit shortage) and a high[Vol. 40, 1997

incidence of parasite infection. This may
apply to infections of both nodular worms
and tapeworms. The possible correlation
between periods of food stress, parasite infection and leaf swallowing needs to be investigated in the future.
Phytochemical hypotheses for chimpanzee leaf swallowing and the pharmacological evidence. Thiarubrine A (Towers
et al., 1985), a powerful antibiotic, antifungal and anthelmintic secondary plant compound was reported by Rodriguez et al.
(1985) to be in the leaves of A. mossambicensis and A. pluriseta. Rodriguez and Wrangham (1993) later proposed that thiarubrine
A in the leaves of A. mossambicensis could
act as a nematocide. Two alternative hypotheses were proposed to explain the function ofswallowing rather than chewing Aspilia
leaves in the presence of thiarubrine A:‘‘buccal absorption’’ (Newton and Nishida,1990) and ‘‘unchewed leaves as thiarubrine
A protective capsules’’ (Rodriguez andWrangham, 1993). Both were proposed ad
hoc to resolve the dilemma of how thiarubrine A would make it to the site of treatment without being destroyed by gastricacids.
However, after numerous attempts to replicate the earlier phytochemical • ndings
Page and colleagues (1992, 1997) could detect no trace of thiarubrine A, B, D, E ortheir corresponding thiophenes in the leavesof 27 samples of three Aspillia species, A.
mossambicensis, A. rudis and A. africana
Pers. C.D., collected from Mahale and Gombein Tanzania; Nanyuki Kenya; the Kampala
District in Uganda, or greenhouse grownspecimens from Vancouver. Furthermore,
analysis of various Aspilia spp. leaves revealed no detectable antifungal activity
against Candida albicans (Page et al., 1997),
a human pathogenic yeast sensitive to thiarubrines (Towers et al., 1985). Messer andWrangham (1995) also found no nematocidal activity against infective L3 stage
Strongyloides nematode larvae in the leaf
extracts of Rubia cordifolia L. (Compositae).
These phytochemical hypotheses have beenabandoned due to lack of any supportive
evidence (Huffman et al., 1996b; Page et al.,1997).

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EVIDENCE FOR SELF-MEDICATION

The possibility has not been completely
abandoned for secondary compounds in theleaves of species being swallowed to havesome effect on intestinal parasites. Becauseof the wide taxonomic variety of plants
swallowed by the African great apes a hypothesis compatible with this idea would
require a common biological activity to be
induced by different secondary compounds.
Support for this comes from in vitro antischistosomal analyses of • ve species from• v e different families known to be swallowed by apes at • v e study sites; Maniophyton fulvum Mull. Arg (Euphorbiaceae), Ipomea involucrata P. Beauv. (Convulvulaceae),
T. orientalis, Lippia plicata Baker (Verbenaceae) and Lagenaria abyssinica (Hook. f.) C.
Jeffrey (Cucurbitaceae) (Table 4). All • ve
species exhibit weak, but similar, inhibitionof movement and egg-laying activity on adultschistosomes (S. japonica) (Ohigashi et al.,in preparation). Speci• c compounds responsible for this action have not yet been isolated.
At present there is no direct evidence from• el d observations to suggest a speci• c rolefor plant secondary compounds in parasite
expulsion via leaf swallowing but the following is offered as speculation for future research. One way that nematode expulsion
may be chemically mediated is by decreasing a worm’s ability to attach itself to themucosal wall of the intestine, making it
more prone to being ‘‘swept out’’ by the samerough whole leaves as they pass through thegut (Huffman et al., 1996b). A variety ofcompounds are known to affect parasite
behavior, and chemical communication occurs between parasites via pheromones
which attract and or repel conspeci• cs (e.g.
Haseeb and Fried, 1988; MacKinnon, 1987;
Salafsky et al., 1984; Sukhdeo and Sukhdeo,1994). Some form of chemotaxis may alternatively explain why worms are attracted into
the folds of the leaves before being expelled(Huffman et al., 1996b).
OTHER POSSIBLE SELF-MEDICATINGBEHAVIORS
Suggestive evidence for other types ofself-medication in non-human primates andin other mammalian species has been reported (see Clayton and Wolfe, 1993; Glan-

189

der, 1994; Hart, 1990). In each case theevidence is variable and most often incomplete but given the wide spread occurrenceof these behaviors across animal taxa they
are brie• y reviewed here.
Fur rubbing
Hypothesis. Fur rubbing is seen in a number of mammalian species including nonhuman primates. Nutritional gain can beignored as the items used in fur rubbing are
not eaten. With regards to its possible medicative function, fur rubbing has been proposed to repel insects and ectoparasites andprovide topical skin treatment for fungal
and bacterial infections.
Behavioral ecology. Fur rubbing is commonly observed in wild and captive capuchin monkeys (Cebus capucinus) and has
been reported for a group of spider monkeys(Ateles geoffroyi) (e.g. Baker, 1996; Buckley,
1983; Oppenheimer, 1968; Richard, 1970;
Ludes and Anderson, 1995). Plant material
can be applied directly or chewed, and mixed
with saliva, rubbed frenziedly into the fur.
Baker (1996) studied fur rubbing in capuchins on the southeastern edge of the Nicoya
Peninsula of Costa Rica. Fifty-three bouts
were observed during a total of 1,140 hours,
i.e., one bout per 19.36 hours. Duration oftime spent fur rubbing ranged from 10 seconds to 41 minutes (mean 6.3 seconds).
Solitary and group rubbing was observed.
Capuchins used at least • ve different plant
genera including fruits of four introduced
Citrus spp. (Rutaceae), the leaves and stemsof Sloanea teni• ora (Elaeocarpuseae), Clematis dioica L (Ranunculaceae) and Pipermarginatum Jacq. (Piperaceae). Citrus(lemon, lime, orange) was the most frequently used genus, but use was often combined with other plant types.
Citrus fruits were used exclusively during
the dry season; however, fur rubbing occurred more often in the rainy season(f � 0.085) than the dry season (f � 0.018).
This seasonal difference was found to besigni• cant (chi square � 15.8, P � 0.05;
Baker, 1996). The trend for an increase in
fur rubbing during the rainy season was
suggested to be related to an increase in risk

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YEARBOOK OF PHYSICAL ANTHROPOLOGY

to bacterial and fungal infection due to a risein temperature and humidity.
Wild Kodiak and brown bears chew theroots of Ligisticum porteri (Umbelliferae)
and then spread their saliva mixed with root
into their fur (Siegstadt, unpublished data
in Cowen, 1990). Captive bears can be induced to exhibit this behavior when presented with these Ligisticum roots or similar pundgent smelling material (J. Siegstadt,
personal communication). Chewing of theroot presumably releases its active compounds and mixes them with saliva for easy
application into the fur or skin below.
White-nosed coatis (Nasua narica) on
Barro Colorado Island, Panama, take thementhol-like smelling resin from freshly
scraped bark of Trattinnickia aspera (Swart)(Burseraceae) and vigorously rub it into
their own fur and/or that of conspeci• cs(Gompper and Holyman, 1993). Grooming
lasts from 30 seconds to 4.5 minutes. Gompper and Holyman note that the practice of
fur rubbing by white-nosed coatis using T.
aspera also occurs elsewhere in Panama.
The pharmacological activity of T. aspera
resin used by coatis is presently unknown.
Phytochemical and ethnobotanical evidence. A number of the plant species observed by Baker (1996) to be used are known
to contain secondary compounds having insecticidal, antiseptic, fungistatic, anti-in• a mmatory, anesthetic, and general dermatological activities. Richard (1970) suggested
that the use of citrus fruits by spider monkeys might repel insects or act as an astringent. All plants share the common quality of
being pungent. Fur rubbing by capuchinsobserved in captivity and elsewhere include
the use of a variety of pungent smellingitems such as tobacco, onions, garlic, millipedes, and formic acid (cf. Baker, 1996).
L. porteri, appropriately called ‘‘bear medicine’’ in parts of western North America, isused as a topical anesthetic and antibacterial by native Americans in the southwest. It
contains volatile and • x ed oils, a lactone
glycoside, an alkaloid, phytosterols, saponins and ferulic acid (Moore, 1979). Navaho
folklore states that revered use of the plant
was taught to them by the bear (Siegstadt,
unpublished data in Cowen, 1990).

[Vol. 40, 1997

Alternative non-medicinal functions for
fur rubbing described above includes thefacilitation of social grooming, thermal regulation, conditioning of the pelage and groupscenting (Baker, 1996; Richard, 1970; Ludes
and Anderson, 1995; Gompper and Holyman, 1993).
Regulation of reproduction
Hypothesis. Plant hormones are known toaffect reproduction in a number of animal
and insect species. Plant secondary compounds and phytoestrogen in the diet ofprimates are proposed to facultatively effectbirth spacing, in• uence the sex of offspring
and regulate fertility.
Behavioral ecology. Glander (1980) was
probably the • rst to suggest a possible link
between the inhibitive effect of plant secondary compounds found in key food resources
and facultative birth spacing. As one possible explanation for the observed interannual variation in birth spacing of howler
monkeys, he suggested that females as awhole may concentrate births seasonally inyears when secondary compound concentration in plant foods are low (high food quality)
and spread births out when concentrations
are high (low food quality). Glander (1994)
has also speculated that chemical components of their diet may allow females toselect the sex of their infant. Speci• c plants
thought to be responsible for the regulationof fertility in howler monkeys have not yet
been identi• ed .
In a 26-month study by Whitten (1983)
the timing of onset, duration and ending of
seasonal mating behavior in female vervet
monkeys (Cercopithecus aethiops) was closely
correlated with the availability and ingestion of the • ow ers of Acacia elatior Brenan(Mimosaceae). Later Garey et al. (1992)
analyzed the • ow ers of this species andfound them to be estrogenic. It was ascertained by Garey and colleagues that theamount of • ow ers consumed by vervet monkeys would provide adequate exogenous estrogen to stimulate the onset of mating
activity.
An in-depth examination of sex and reproduction in the Gombe chimpanzees by Wallis(1995, 1997) noted signi• ca nt seasonal pat-̶ 280 ̶

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EVIDENCE FOR SELF-MEDICATION

terns in a number of reproductive parameters including conception, anogenital swelling, infant mortality and fertility. Diet waspredicted to be a mediating factor (Wallis,
1992, 1994). In particular, phytoestrogen
induced fertility regulation as a consequence of intensive foraging on seasonallyavailable plant foods was proposed (Wallis,
1997).
Pharmacological evidence. Phytochemical data supporting or rejecting plant based
reproductive control in non-human primates are scarce. With regards to the great
apes, the presence of two active diterpenes(kaurenoic and grandi• ornenic acid) in Aspilia spp. collected from Mahale and Gombe
have been reported (Huffman et al., 1996b;
Page et al., 1992). Page et al. (1992) foundthat both compounds exhibited uterostimulatory activity on in vitro oestrogenized female guinea pig uterine tissues. Potent
uterotonic activity of kaurenoic and grandiflornenic acids has also been reported elsewhere (Gallegos, 1985; Ponce-Monter et al.,1983). Page suggested that ingestion of theleaves might have a secondary effect on
reproduction in female chimpanzees ingesting the leaves of Aspilia spp. plants. However, it is not known if the compounds areavailable to chimpanzees in signi• cantamounts or whether the typical form ofingestion of Aspilia leaves (swallowing wholewithout chewing) allows for their appropriate release into the body.
A number of invertebrates, such as butter• y species of the family Lepidoptera, aredependent upon plant secondary compounds,
such as pyrrolizidine alkaloid precursor in
Helioptropium sp. (Boraginaceae), to produce sex hormones essential for reproduction (Chapman and Blaney, 1979). Plant
secondary compounds found in the diet ofsome mammals too are suggested to either
trigger or inhibit ovulation and conception(e.g. Berger et al., 1977; Starker, 1976; Sadlier, 1969). Throughout history humans have
utilized a number of plant hormones tosuppress and enhance their reproductive
and sexual activity (Lewis and Elvin-Lewis,1977). To date, however, detailed non-human primate studies combining both behavioral ecology and phytochemistry have not191

been published. This is an extremely exciting area wide open for research.
MEDICINAL PLANT SELECTION:
ORIGINS, MECHANISMS OF
TRANSMISSION, AND LEARNING
The diversity of plant taxa selected byapes for possible self-medication is likely to
be in• uenced by the ecological and geographical diversity of the habitats represented (Table 2), yet a pattern emerges fromthe species known to be selected by apes
across Africa for bitter pith chewing and leaf
swallowing. Apes of the same species inadjacent groups or regional populations tend
to use many of the same or related plant
species. The same or related plant species
are also selected by different ape species inneighboring, regional and intra-regional
populations (see Table 3, 4). This would
suggest that all ape species are using acommon criteria when they select plants for
self-medication.
Origins of self-medicative behaviors, plantselection criteria as a product of function
The similarity of plants selected by neighboring populations of the same species may
represent localized cultural traditions, maintained in part by information exchange via
female group transfer (cf. Huffman andWrangham, 1994; Matsuzawa and Yamakoshi, 1996). However, the use of one plant
species by two sympatric ape species neednot be explained by inter-species interactions, although the possibility of interspecies exchange of information about theenvironment is well worth looking into. Similarly, the selection of a common plant species
by two chimpanzee sub-species inhabiting
two different ends of the continent does notmean that they share an ancestral artifact ofplant species preference. Instead, both cases
most likely represent the convergence ofplant selection criteria for rough hairy surfaces as determined by the function of leafswallowing behavior itself.
In this light, the selection of plants used inassociation with bitter pith chewing may
also be based on chemosensory criteria inherent in the function of the behavior itself.
There may be ‘‘associative predispositions’’(see Revusky, 1984) for the association of̶ 281 ̶

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YEARBOOK OF PHYSICAL ANTHROPOLOGY

tastes and smells that direct organisms intheir search and learning processes about
what makes one feel better. Bitter taste
perception thresholds vary among nonhuman primate species, as they certainly do
among human cultures, (cf. Hladik and Simmen, 1996) but bitter taste is a reliable
signal of toxicity (Table 1). A number of
secondary compounds ubiquitous in natureare bitter tasting (saponins, alkaloids andsome sesquiterpenoids, terpenoids and steroid glycocides) and many possess important pharmacological activity (Table 1; cf.
Crellin and Philpott, 1990; Githens, 1949;
Shiba, 1976).
Historically, herbalists have emphasized
the importance of taste and smell in theevaluation of plant medicinal properties (cf.
Crellin and Philpott, 1990). In a study of thecriteria of medicinal plant selection by theTzeltal Mayans of Highland Chiapas in
Mexico, Brett (1994) noted that taste andsmell were consistently used to select orevaluate a plant to treat ethnomedicallyrelated illnesses. Regardless of taxonomy,
bitter tasting plants were selected and predominantly used to treat gastrointestinal
upsets, parasites and stomach pains (Brett,1994). A number of bitter Vernonia species
found across Africa and Central America,
just to name a few examples, are known
both for their wide ethnomedicinal use andpharmacological effectiveness against gastrointestinal related ailments, including parasitosis (e.g. Berlin and Berlin, 1996; Huffman et al., 1996a).
Individual acquisition of self medicative
behaviors
Perhaps one of the most challenging questions which needs to be investigated is theway in which proposed self-medicative behaviors are individually acquired. The suggestion that self-medication is a behavioral
tradition includes a range of possibilities for
how the behavior started and how individuals become predisposed to ingest medicinal
plants. At one extreme, animals may havean innate tendency to select appropriate
plants when ill, so that the role of tradition
is reduced to local enhancement (i.e., naive
individuals have their attention drawn tospecies used by others) (Huffman and Wrang-[Vol. 40, 1997

ham, 1994). However, in the case of leaf
swallowing and bitter pith chewing it is notjust what species is being ingested, but also
what parts and how they are ingested thatmust be learned for the behavior to beeffective and sometimes even for the plant tobe safe to ingest. At the other extreme,
chimpanzees may be averse to bitter piths
and rough leaves. Given the high degree ofconservatism in chimpanzee feeding habits(Nishida, 1987) random sampling of novel
food items, especially when ill, does notseem likely to occur very frequently. If so,
traditions must have started rarely, perhaps
as a result of ill, hungry chimpanzees trying
new foods during periods of extreme foodscarcity, recovering their health, and associating their improved health with the new
item.
Selective association between taste andgastrointestinal illness is a widely accepted
principal of taste aversion learning among
mammals (cf. Revusky, 1984) and the learning mechanism of food aversion in response
to induced sickness has been well documented in a number of animal species (seeZahorik and Albro Houpt, 1977). While thehighly adaptive signi• ca nce of this reversed
process, i.e., being able to associate improved health with the ingestion of novel
plants having medicinal properties, seems
self-evident, such learning mechanisms havereceived little attention (cf. Zahorik, 1977)
and is an area greatly in need of further
research.
Important bene• t s come from social learning which allows naive individuals to acquire information through the experience ofothers, and over time to perfect the behavior
themselves (see Hikami et al., 1990; Huffman, 1996; Fragazy and Visalberghi, 1996;
Galef, 1977; Nishida, 1987; Inoue-Nakamura and Matsuzawa, 1997). Once an effective self-medicative behavior is recognized,
perhaps it spreads through the group, • rst
slowly, but after a time increasingly fasteras it is passed onto the youngest members of
the group. At this stage, it may be just one
more part of the mother’s foraging and behavioral repertoire to be acquired. At Mahale, and presumably elsewhere, initial exposure to self-medicative behaviors takes
place by individuals at an early age, not̶ 282 ̶

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EVIDENCE FOR SELF-MEDICATION

when ill themselves, but by observing the
behavior of those that are ill, usually theirmothers (Huffman and Wrangham, 1994).
Young chimpanzees have been observed on
several occasions to closely watch these behaviors and immediately thereafter attempt
to perform them themselves (see Huffman
and Seifu, 1989; Huffman and Wrangham,
1994).
It is of considerable interest to know justto what extent primates are able to use
social input to guide their appropriate choice
and use of plants. For example, when ingesting the bitter pith of V. amygdalina, chimpanzees selectively remove the leaves andbark before ingesting the inner pith’s bitter
juices. In this way they avoid any signi• cantintake of the toxic sesquiterpene lactones
abundant in the leaves and bark, in favor of
the more host friendly steroid glucosides.
Humans have learned to use the leaves ofV. amygdalina in moderation when mixing
them with fodder for horses and other livestock as a de-wormer, or when they use theleaves themselves as medicine or in tonic
foods (Huffman et al., 1996a). In striking
contrast, domestic livestock do not appear
to forage selectively or in moderation on
V. amygdalina leaves, and the outcome isoften lethal. Among the Temme of Sierra
Leone, V. amygdalina is known as ‘‘a-difwir’’ which means ‘‘kill goats’’ (Burkill, 1985).
The problem has obviously been around longenough for the plant to get this name, inspite of which goats seem not to have learned
to avoid it. This may be due to the lack of an
intact stable social group caused by herding
practices of separating mother from youngwhen foraging, whereby grazing aversions
are not passed on from mother to infant.
A troop of Japanese macaques released
into the semi-desert brushland of southern
Texas learned to avoid the neurotoxic berries and leaves of Karwinsinski humboldtiana (Roemer & Schultes) Zucc. (Rhamnaceae) after eight individuals died and others
suffered temporary paralysis from it (Fedigan, 1991). The troop was still adapting to a
new environment and was feeding off many
novel plant species available in the new
habitat. This alone could make it quitedifficult for one individual to identify theplant(s) responsible for its illness and avoid

193

it, let alone for other members not afflictedwith paralysis to do so, too. Once preferences change, however, rapid social transmission among troop members occurs (Hikami
et al., 1990).
FUTURE DIRECTIONS AND PRACTICALAPPLICATIONS
Some basic guidelines and predictions
The evidence described in this review forprimates and other animal taxa suggeststhat a variety of behavioral adaptations
exist for the control of internal and possibly
external parasites. Much of the detailed
evidence in support of the developing hypotheses on self-medication in the African great
apes comes from their response to changing
levels of parasite infection. This model should
be applicable to other primate species infected with parasites exhibiting seasonal
reproduction or reinfection. Other in• uences are likely to be operating and their
possibility should not be ignored.
Systematic monitoring of individuals (notpopulations) throughout the year for • uct uating levels of parasite infection is an effective means of identifying the predominantparasites and their likely period of increased
impact on the host (Huffman et al., 1997).
Close long-term monitoring of the health ofgroup members using detailed analysis ofactivity budgets (resting time, rate of locomotion, feeding time, etc.) and systematic inspection of general health signs (e.g. diarrhea, coughing, runny nose, etc.) is necessary
to identify illness when it occurs and tounderstand the proximate effects off that
illness on the individual as well as thefunction and effectiveness of any proposed
self-medicative behavior. These procedures
are straight forward and compatible withmost primate • el d study designs.
Intestinal parasites are by no means the
only in• uences responsible for ill health.
Other sources of pathogens need to be investigated which may involve the capture andcontainment of animals for the collection ofblood and tissue samples. The effects ofintervention on observer/subject relations is
a concern. It will be necessary to develop
techniques to work around these difficulties.
There are limitations as to what can bedone in the • eld and increased collaboration

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YEARBOOK OF PHYSICAL ANTHROPOLOGY

between colleagues from the applied animaland plant sciences (e.g. veterinary medicine,
pharmacology, natural plant product chemistry) is essential in any attempt to fully
understand the implications of a proposed
self-medicative behavior. The multi-disciplinary research conducted at Mahale by The
C.H.I.M.P.P. Group (Chemo-ethology of
Hominoid Interactions with Medicinal Plants
and Parasites) is one example of how thishas been effectively achieved in some areas(see Huffman, 1994; Jacobsen and Hamel,
1996).
Three of the greatest constraints on • eld
investigations of self-medicative behavior
are 1) the unpredictability of the behaviors’
occurrence, 2) unreliability of being able toconsistently follow and observe sick individuals over time, and 3) restraints on experimental manipulation. In order to test a numberof the ideas evolving from the developing
hypotheses of self-medication, these constraints must be overcome. For example,
through the safe and controlled introductionof medicinal plants to captive primate socialgroups, it may be possible to evaluate someof the criteria of medicinal plant selectionand • nd out how individual acquisition andgroup transmission occurs. Just one of theimportant questions begging to be answeredis how do naive captive apes respond to theputative medicinal plants of their wild conspeci• cs? If ill and infected with nematodes,
would they swallow rough hairy leaves andchew bitter pith or ignore them completely?
Investigations into the potential for selfmedicative behavior in captive zoo primatesor other animals can be expected to greatly
advance our understanding of what goes onin the wild and may provide importantbene• ts to captive animals.
Herbal medicine and environmental
enrichment in zoos
According to Jan Vermeer (Primate
Keeper), since 1985 a pioneering project
introducing herbal medicine into captive
primate exhibits has been underway at the
Apenheul Zoo in Holland (Vermeer, 1995).
After determining some of the major healthproblems of the woolly monkey (Lagothrix
lagotricha) population at the zoo, herb gardens were planted in plots and covered with

[Vol. 40, 1997

wire mesh. The mesh is set high enoughabove the ground to prevent primates fromcompletely destroying the plants, but low
enough to allow access to the distal branchesof herbs as forage. Among the plants reported to be used are several common European herb species noted for their activity
against stress (Wild Chamomile (Matricaria
chamonilla (Linn.) (Compositae); Catnip
Nepeta cataria (Linn.) (Labiatae); Lavender
Lavendula augustifolia (Labiatae)), hypertension (Garlic Allium sativum (Linn.) (Liliaceae); Hawthorn Crataegus oxyacantha(Linn.) (Roseaceae)) and bladder infection(Common Berberry Berberis vulgaris (Linn.)(Berberidaceae); Fennel Foeniculum vulgari(Gaert.) (Umbelliferae)). The actual effectsof these plants on the health of the woollymonkeys have not yet been clinically evaluated.
A similar project was begun at the Denver
Zoo in Colorado in 1996 under the directionof Merle Moore (Program Administrator,
Horticulture and Landscape Maintenance).
Wire mesh gardens similar to those used at
Apenheul have been placed in the gorillaand orangutan outdoor exhibits at the zoo’s
new Primate Panorama exhibit. Beyond thepotential for providing health promoting
herbs and educational awareness about theuse of medicinal plants by primates in thewild, these two programs exemplify new andinnovative ways of maintaining a selfsustaining source of environmental- and dietenrichment in zoo exhibits (Vermeer, 1995).
Further studies are encouraged to evaluate
locally available plants for use also in thezoos of developing countries around theworld.
Sustainable resources of medicine forlivestock in developing countries
One future direction in sight for the • el dof self-medication is the application of knowledge gained about medicinal plants andtheir uses to the human and veterinary
medical sciences. Oesophagostomum spp. infections are common in non-human primates, pigs, sheep, cattle and occasionally
humans, and are considered signi• cantpathogens (cf. Anderson, 1992; Brack, 1997;
Polderman et al., 1991). While a number ofbroad spectrum anthelmintics are currently

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available for the treatment of livestock, growing chemoresistance to these anthelmintics
and the prohibitive costs of such drugs torural livestock owners and zoological parks
in developing African nations make theiruse impractical if not at times impossible(Jackson, 1993; Mathias et al., 1996; Roepstorff et al., 1987).
Recently, great interest has been taken inlooking for new ways of treatment using
natural plant products derived from ethnomedicine (cf. Kasonia and Ansay, 1994; McCorkle et al., 1996; Bøgh et al., 1996). The
study of self-medication in great apes too
can be expected to provide equally viable
sources of natural products for the effective
treatment of parasitosis in humans, domestic and captive animals (Berry et al., 1995).
Based on the results of work at Mahale, ajoint effort between the Danish Centre forExperimental Parasitology (The Royal Veterinary and Agricultural University, Copenhagen), the Sokoine University of Agriculture (Morogoro, Tanzania), The Universityof Dar es Salaam (Dar es Salaam, Tanzania)
and the author is being made to determine
the in vitro efficacy of these plants against
Oesophagostomum infections in swine under controlled laboratory conditions. This
will allow for the controlled testing of thebitter pith chewing and leaf swallowing
nematode control hypotheses in apes and toaccess the potential of these endemic, readily
available and sustainable plants as sourcesof antiparasitics in Africa.
Expectations for the future
Further • el d and laboratory research into
self-medicative behavior in other primate
species is strongly encouraged. As this review has shown, answers to a few questions
invariably lead to more questions. As more
researchers in the • el d begin to look forsimilar types of behavior, they will be foundand more answers will be provided. Becauseof the obvious adaptive signi• ca nce of selfmedication, its existence is predicted to be
wide-spread. Other types of self-medicative
behavior are predicted to occur in the great
apes as well as in monkeys and prosimians.
The challenge is in • nding what the immediate threats to health and survival are in a

195

population and by what means they aredealt with by that particular species.
The use of dietary clay by humans todetoxify food plants high in secondary compound content is considered to have expanded the availability of food to modern
humans beyond that which was available toour prehominid ancestors (Johns, 1990).
From golden bamboo lemurs to apes, thefrequent ingestion of clay soils among primates may also play an important role inallowing primates to widen their dietary
repretoir, especially at certain critical timesof the year. The strong similarities in plantselection criteria among the African great
apes and the common use of some plants bychimpanzees and humans for similar illnesses is tantalizing evidence for the evolution of self-medication. In this light, ourhominid ancestors can be predicted to haveexhibited some similarities in plant selection criteria with both extant apes and modern humans. The fossil record provides nodirect evidence for the • ner subtleties of
feeding behavior and diet, but it seems
reasonable to hypothesize that early
hominids would have displayed at least therange of extant ape self-medicative behaviors.
Whether it be chimpanzees selectively
ingesting plants in ways that lead to theseasonal expulsion of certain parasites orthe in• uence of phenology and diet on theonset of mating in female vervet monkeys,
the complexity of primate, parasite, andplant interactions cannot be denied. Studyof these interactions in the framework of
self-medication provide a new and entirely
novel level of complexity to our understanding of primate behavioral ecology.
ACKNOWLEDGMENTS
I give my sincere gratitude to the Government of Tanzania for the long-term cooperation and commitment extended to myself
and colleagues at Mahale and Gombe. In
particular, I am thankful to the TanzanianNational Scienti• c Research Council, Tanzanian National Parks, Serengeti Wildlife Research Institute, Mahale Mountains Wildlife Research Centre and Gombe Stream
Research Centre. My deepest gratitude goesto all my colleagues and • eld assistants for̶ 285 ̶196

YEARBOOK OF PHYSICAL ANTHROPOLOGY

their generous contributions of yet unpublished data and personal communications.
Without their advise, support, and understanding, this review would not have beenpossible. I sincerely thank (in alphabeticalorder) G. Balansard, A.K. Basabose, J.P.
Berry, C. Boesch, D.A. Collins, B. Gilbert, J.
Goodall, J. Holmes, J. Itani, M.S. Kalunde,
K. Koshimizu, S. Kuroda, H. Ohigashi, J.
Page, K. Strier, Y. Sugiyama, H. Takemoto,
G.H.N. Towers, L.A. Turner, J. Yamagiwa,
and G. Yamakoshi for their generous collaboration and comments. Research done in 1987,
1989, and 1990–91, 1993–94, and 1995–96
in the • eld that is mentioned in this paper
was supported by a grant under the Monbusho International Scienti• c Research Program to T. Nishida (61043017, 62041021,
63043017, 03041046) and by travel and research grants from the Plant Science Research Foundation, Kyoto University, and
the Wellcome Trust, U.K. Technical advise
and support was provided by staff of theLouis Pasteur Center for Medical Research,
Kyoto, in particular T. Kishida and K. Uno. I
express my sincere appreciation to the Govenors and staff of the Wellcome Trust for theirkindness and understanding, in particular
Sir R. Gibbs and R.E. Howells. In closing, I
thank my partner in life, F. Naito, for her
unwavering support and encouragement of
my quest for answers and for sharing in thehardships and happiness of pursuing mydreams.
LITERATURE CITED
Abbiw DK (1990) Useful Plants of Ghana. Kew: Intermediate Technology Publications and Royal Botanic Gardens.
Allison AC (1982) Co-evolution between hosts and infectious disease agents and its effect on virulence. In RM
Anderson and RM May (eds.): Population Biology of
Infectious Diseases. Berlin: Springer-Verlag, pp. 245–
267.
Anderson RC (1992) Nematode Parasites of Vertebrates.
Their Development and Transmission. Walingford:
C.A.B. International.
Anderson RM, and May RM (1982) Population Biology of
Infectious Diseases. Berlin: Springer-Verlag.
Asaka Y, Kubota T, and Kulkarni AB (1977) Studies on abitter principle from Vernonia anthelmintica. Phytochemistry 16:1838–1839.
Baker M (1996) Fur rubbing: Use of medicinal plants by
capuchin monkeys (Cebus capucinus). Am. J. Primatol. 38:263–270.
Barnard CJ, and Behnke JM (1990) Parasitism andHost Behaviour. London: Taylor and Francis.

[Vol. 40, 1997

Barrows M (1996) A survey of the intestinal parasites ofthe primate in Budongo Forest, Uganda. Report to theDept. of Veterinary Medicine, University of Glasgow.
Beaver PC, Jung RC, and Cupp EW (1984) Clinical
Parasitology. 9th ed. Philadelphia: Lea and Febiger.
Behnke JM (1987) Evasion of immunity by nematodeparasites causing chronic infections. Adv. Parasitol.
26:1–71.
Berger PJ, Sanders EH, Gardner PD, and Negus NC(1977) Phenolic plant compounds functioning as reproductive inhibitors in Microtus montanus. Science 195:
575–577.
Berlin EA, and Berlin B (1996) Medical Ethnobotany of
the Highland Maya of Chiapas, Mexico: The Gastrointestinal Diseases. Princeton, NJ: Princeton University Press.
Berry JP, McFarren MA, and Rodriguez E (1995) Zoopharmacognosy: A ‘‘Biorational’’ strategy for phytochemical prospecting. In DL Gustine and HE Flores(eds.) Phytochemicals and Health. Rockville: American Society of Plant Physiologist, pp. 165–178.
Boesch C (1995) Innovation in wild chimpanzees (Pantroglodytes). Int. J. Primatol. 16:1–16.
Bøgh HO, Andreassen J, and Lemmich J (1996) Anthelmintic usage of extracts of Embelia schimperi from
Tanzania. J. Ethnopharmacol. 50:35–42.
Brack M (1987) Agents Transmissible from Simians toMan. Berlin: Springer-Verlag.
Brett JA (1994) Medicinal Plant Selection Criteria among
the Tzeltal Maya of Highland Chiapas, Mexico. Doctoral dissertation, University of California, San Francisco.
Brooks DR, and McLennan DA (1993) Parascript: Parasites and the Language of Evolution. Washington, DC:
Smithsonian Institution Press.
Buckley JS (1983) The feeding behavior, social behavior,and ecology of the white-faced monkey Cebus capucinus at Trujillo, northern Honduras, Central America.
PhD thesis, University of Illinois, Urbana. Ann Arbor:
University Micro• l ms.
Burkill HM (1985) The Useful Plants of West Tropical
Africa. 2nd ed., Vol 1. Kew: Royal Botanical Gardens.
Choquette LPE, Gibson GG, and Pearson AM (1969)
Helminths of the grizzly bear Ursus arctos in northern
Canada. Can. J. Zool. 47:167–170.
Chapman RF, and Blaney WM (1979) How animals
perceive secondary compounds. In GA Rosenthal and
DH Janzen (eds.): Herbivores, their interactions withsecondary plant metabolites. New York: Academic, pp.
161–198.
Clayton DH, and Wolfe ND (1993) The adaptive signi• cance of self-medication. TREE 8:60–63.
Cowen R (1990) Medicine on the wild side. Science News138:280–282.
Crellin JK, and Philpot J (1990) Herbal Medicine Past
and Present Vol. 2. A Reference Guide to Medicinal
Plants. Durham: Duke University Press.
Dalziel JM (1937) The Useful Plants of West Tropical
Africa. In J Hutchinson and JM Dalziel (eds.): Appendix to Flora of West Tropical Africa. London: Whitefriars Press.
Davies ND, and Baillie IC (1988) Soil-eating inred leafmonkeys (Presbytis rubicunda) in Saba, northern
Borneo. Biotropica 20:252–258.
Ehrlich P, and Raven PH (1964) Butter• ies and plants:
A study in coevolution. Evolution 18:586–608.
Ewald PW (1994) Evolution of Infectious Disease. Oxford: Oxford University Press.
Fedigan LM (1991) History of the Arashiyama WestJapanese Macaques in Texas. In LM Fedigan and PJ
Asquith (eds.): The Monkeys of Arashiyama. Thirty• v e Years of Research in Japan and the West. Albany:
State University of New York Press, pp. 54–73.

̶ 286 ̶

Huffman]

EVIDENCE FOR SELF-MEDICATION

Feeny P (1976) Plant apparency and chemical defense.
Recent advances in phytochemistry 10:1–40.
File SK, McGrew WC, and Tutin CEG (1976) The
intestinal parasites of a community of feral chimpanzees, Pan troglodytes schweinfurthii. J. Parasitol.
62:259–261.
Fragazy DM, and Visalberghi E (1996) Social learning inmonkeys: Primate ‘‘primacy’’ reconsidered. In CM
Heyes and BG Galef (eds.): Social Learning in Animals: The Roots of Culture. San Diego: Academic, pp.
65–84.
Freeland WF, and Janzen DH (1974) Strategies inherbivory by mammals: The role of plant secondary
compounds. Am. Naturalist 108:269–289.
Futuyma DJ, and Slatkin M (1983) Coevolution. Sunderland: Sinauer.
Galef BG (1977) Mechanisms for the social transmissionof acquired food preferences from adult to weanlingrats. In LM Barker, MR Best, and M Domjan (eds.):
Learning Mechanisms in Food Selection. Baylor, TX:
Baylor University Press, pp. 123–148.
Gallegos AJ (1985) The zoapatle. VI. Revisited. Contraception 31:487–497.
Garey J, Markiewicz L, and Gurpide E (1992) Estrogenic • ow ers, a stimulus for mating activity in female
vervet monkeys. In XIVth Congress of the International Primatological Society Abstracts, Strassbourg,p. 210.
Gasquet M, Bamba D, Babadjamian A, Balansard G,
Timon-David P, and Metzger J (1985) Action amoebicide et anthelminthique du vernolide et del’hydroxyvernolide isoles des feuilles de Vernonia colorata (Willd.) Drake. Europ. J. Med. Chem. Theory,
2:111–115.
Githens TS (1949) Drug Plants of Africa. Philadelphia:
University of Pennsylvania Press.
Glander KE (1975) Habitat description and resource
utilization: A preliminary report on mantled howler
monkey ecology. In R.H. Tuttle (ed.): Socioecology andPsychology of Primates. The Hague: Mouton, pp.
37–57.
Glander KE (1980) Reproduction and population growthin free-ranging mantled howling monkeys. Am. J.
Phys. Anthropol. 53:25–36.
Glander KE (1982) The impact of plant secondary
compounds on primate feeding behavior. Yrbk. Phys.
Anthropol. 25:1–18.
Glander KE (1994) Nonhuman primate self-medication
with wild plant foods. In NL Etkin (ed.): Eating on theWild Side: The Pharmacologic, Ecologic, and Social
Implications of Using Noncultigens. Tuscon: University of Arizona Press, pp. 239–256.
Glander KE, Wright PC, Seigler DS, Randrianasolo V,
and Randrianasolo B (1989) Consumption of cyanogenic bamboo by a newly discovered species of bamboo
lemur. Am. J. Primatol. 19:119–124.
Gompper ME, and Holyman AM (1993) Grooming with
Trattinnickia resin: Possible pharmaceutical plant
use by coatis in Panama. J. Trop. Ecol. 9:533–540.
Halstead JA (1968) Geophagia in Man: Its Nature andNutritional Effects. Am. J. Clin. Nutr. 21:1384–1393.
Hamilton WD (1964a) The genetical evolution of social
behavior. I. J. Theoret. Biol. 7:1–16.
Hamilton WD (1964b) The genetical evolution of social
behavior. II. J. Theoret. Biol. 7:17–52.
Hamilton WD, and Zuk M (1982) Heritable true • t nessand bright birds: A rule for parasites? Science 218:384–
387.
Hart BL (1990) Behavioral adaptations to pathogens
and parasites: Five strategies. Neurosci. Biobehav.
Rev. 14:273–294.
Haseeb MA, and Fried B (1988) Chemical communication in helminths. Adv. Parasitol. 27:169–207.

197

Hikami K, Hasegawa Y, and Matsuzawa T (1990) Socialtransmission of food preferences in Japanese monkeys(Macaca fuscata) after mere exposure or aversion
training. J. Comp. Psychol. 104:233–237.
Hladik CM (1977a) Chimpanzees of Gabon and chimpanzees of Gombe: Some comparative data on the diet. In
TH Clutton-Brock (ed.): Primate Ecology. London:
Academic, pp. 481–502.
Hladik CM (1977b) A comparative study of the feeding
strategies of two sympatric species of leaf monkeys:
Presbytis senex and Presbytis entellus. In TH CluttonBrock (ed.): Primate Ecology. London: Academic, pp.
324–353.
Hladik CM, and Simmen B (1996) Tast perception andfeeding behavior in nonhuman primates and humanpopulations. Evol. Anthropol. 5:58–71.
Holmes JC, and Zohar S (1990) Pathology and host
behavior. In CJ Barnard and JM Behnke (eds.):
Parasitism and Host Behavior. London: Taylor andFrances, pp. 34–63.
Howe HF, and Westley LC (1988) Ecological relationships of plants and animals. New York: Oxford University Press.
Huffman MA (1993) An investigation of the use of
medicinal plants by wild chimpanzees. Current status
and future prospects. Primate Res. 9:179–187.
Huffman MA (1994) The C.H.I.M.P.P. Group: A multidisciplinary investigation into the use of medicinal
plants by chimpanzes. Pan Africa News 1:3–5.
Huffman MA (1996) Acquisition of innovative cultural
behaviors in nonhuman primates: A case study ofstone handling, a socially transmitted behavior inJapanese macaques. In CM Heyes and BG Galef Jr(eds.): Social Learning in Animals: The Roots ofCulture. San Diego: Academic, pp. 267–289.
Huffman MA, and Seifu M (1989) Observations on theillness and consumption of a possibly medicinal plant
Vernonia amygdalina (Del.), by a wild chimpanzee inthe Mahale Mountains National Park, Tanzania. Primates 30:51–63.
Huffman MA, and Wrangham RW (1994) The diversityof medicinal plant use by chimpanzees in the wild. In
RW Wrangham, WC McGrew, FB deWaal and PG
Heltne (eds.): Chimpanzee Cultures. Cambridge, MA:
Harvard University Press, pp. 129–148.
Huffman MA, Nishida T, and Uehara S (1990) Intestinal
parasites and medicinal plant use in wild chimpanzees: Possible behavioral adaptation for the control ofparasites. Mahale Mountains Chimpanzees Research
Project. Ecological Report no. 72. Kyoto: Kyoto University.
Huffman MA, Gotoh S, Izutsu D, Koshimizu K, andKalunde MS (1993) Further observations on the use of
Vernonia amygdalina by a wild chimpanzee, its possible effect on parasite load, and its phytochemistry.
African Study Monographs 14:227–240.
Huffman MA, Koshimizu K, and Ohigashi H (1996a)
Ethnobotany and zoopharmacognosy of Vernonia
amygdalina, a medicinal plant used by humans andchimpanzees. In PDS Caligari and DJN Hind (eds.):
Compositae: Biology and Utilization. Vol 2. Kew: The
Royal Botanical Gardens, pp. 351–360.
Huffman MA, Page JE, Sukhdeo MVK, Gotoh S, Kalunde MS, Chandrasiri T, and Towers GHN (1996b)
Leaf-swallowing by chimpanzees, a behavioral adaptation for the control of strongyle nematode infections.
Int. J. Primatol. 72:475–503.
Huffman MA, Gotoh S, Turner LA, Hamai M, andYoshida K (1997) Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates
38:111–125.

̶ 287 ̶198

YEARBOOK OF PHYSICAL ANTHROPOLOGY

Idani G, Kuroda S, Kano T, and Asato R (1994) Flora andvegetation of Wamba Forest, Central Zaire with reference to Bonobo (Pan paniscus) foods. TROPICS 3:309–
332.
Inoue-Nakamura N, and Matsuzawa T (1997) Development of stone tool use by wild chimpanzees (Pantroglodytes). J. Comp. Psychol. 111:159–173.
Jackson F (1993) Anthelmintic resistance. The state ofplay. Br. Vet. J. 149:1233–1235.
Jacobsen L, and Hamel R (1996) International Directoryof Primatology. Madison: Wisconsin Regional Primate
Research Center.
Janzen DH (1978) Complications in interpreting thechemical defenses of trees against tropical arboreal
plant-eating vertebrates. In GG Montgomery (ed.):The Ecology of Arboreal Folivores. Washington, DC:
Smithsonian Institute Press, pp. 73–84.
Jisaka M, Kawanaka M, Sugiyama H, Takegawa K,
Huffman MA, Ohigashi H, and Koshimizu K (1992a)
Antischistosomal activities of sesquiterpene lactones
and steroid glucosides from Vernonia amygdalina,
possibly used by wild chimpanzees against parasiterelated diseases. Biosci. Biotech. Biochem. 56:845–
846.
Jisaka M, Ohigashi H, Takagaki T, Nozaki H, Tada T,
Hirota M, Irie R, Huffman MA, Nishida T, Kaji M, andKoshimizu K (1992b) Bitter steroid glucosides, vernoniosides A1, A2, and A3 and related B1 from a possible
medicinal plant Vernonia amygdalina, used by wild
chimpanzees. Tetrahedron 48:625–632.
Jisaka M, Ohigashi H, Takegawa K, Hirota M, Irie R,
Huffman MA, and Koshimizu K (1993a) Steroid glucosides from Vernonia amygdalina, a possible chimpanzee medicinal plant. Phytochemistry 34:409–413.
Jisaka M, Ohigashi H, Takegawa K, Huffman MA, andKoshimizu K (1993b) Antitumor and antimicrobialactivities of bitter sesquiterpene lactones of Vernonia
amygdalina, a possible medicinal plant used by wild
chimpanzees. Biosci. Biotech. Biochem. 57:833–834.
Johns T (1990) With Bitter Herbs They Shall Eat It.
Tucson: The University of Arizona Press.
Kasonia K, and Ansay M (1994) Métissages en santé
animale de Madagascar a Haiti. Namur: Presses
Universitaires de Namur.
Kawabata M, and Nishida T (1991) A preliminary noteon the intestinal parasites of wild chimpanzees of theMahale Mountains, Tanzania. Primates 32:275–278.
Kloos H, and McCullough FS (1987) Plants with recognized molluscicidal activity. In KE Mott (ed.): Plant
Molluscicides, New York: John Wiley and Sons, pp.
45–108.
Koshimizu K, Ohigashi H, Huffman MA, Nisihda T, andTakasaki H (1993) Physiological activities and theactive constituents of potentially medicinal plants
used by wild chimpanzees of the Mahale Mountains,
Tanzania. Int. J. Primatol. 14:345–356.
Krepel HP, Baeta S, Kootstra CJ, and Polderman AM(1995) Reinfection patterns of Oesophagostomum bifurcum and hookworm after anthelmintic treatment.
Trop. Geogr. Med. 47:160–163.
Kreulen DA (1985) Lick use by large herbivores: A
review of bene• ts and banes of soil consumption.
Mammal Rev. 15:107–123.
Kreulen DA, and Jager T (1984) The signi• c ance of soil
ingestion in the utilization of arid rangelands by large
herbivores with special reference to natural licks on
the Kalahari pan. In FMC Gilchrist and RI Mackie(eds.): Herbivore Nutrition in the Subtropics andTropics. Johannesburg: The Science Press, pp. 204–
221.
Kupchan SM, Hemingway RJ, Karim A, and Werner D(1969) Tumor Inhibitors XLVII. vernodalin and vernomygdin, two new cytotoxic sesquiterpene lactones[Vol. 40, 1997

from Vernonia amygdalina Del. J. Organic Chem.
34:3908–3911.
Lewis WH, and Elvin-Lewis MPF (1977) Medical Botany.
New York: John Wiley and Sons.
Ludes E, and Anderson JR (1995) ‘Peat-bathing’ bycaptive white-faces capuchin monkeys (Cebus capucinus). Folia Primatol. 65:38–42.
Luque MH, and Stokes AW (1976) Fishing behaviour of
Alaskan brown bears. Bear Res. Management 3:71–
78.
MacKinnon BM (1987) Sex attractants in nematodes.
Parsitol. Today, 3:156–158.
Mahaney WC, Watts DP, and Hancock RGV (1990)
Geophagia by mountain gorillas (Gorilla gorillaberingei) in the Virunga Mountains, Rwanda. Primates 31:113–120.
Mahaney WC, Hancock RGV, and Aufreiter S (1995a)
Mountain gorilla geophagy: A possible strategy for
dealing with intestinal problems. Int. J. Primatol.
16:475–487.
Mahaney WC, Stambolic A, Knezevich M, Hancock RGV,
Aufreiter S, Sanmugadas K, Kessler M, and Grynpas
M (1995b) Geophagy amongst Rhesus macaques on
Cayo Santiago, Puerto Rico. Primates 36:323–333.
Mahaney WC, Hancock RGV, Aufreiter S, and Huffman
MA (1996) Geochemistry and clay minerology of termite mound soil and the role of geophagy in chimpanzees of the Mahale Mountains, Tanzania. Primates
37:121–134.
Mahaney WC, Milner MW, Sanmugadas K, Hancock
RGV, Aufreiter S, Wrangham RW, and Pier HW (1997)
Analysis of geophagy soils in Kibale forest, Uganda.
Primates 38:159–176.
Mathias E, McCorkle CM, and Schillhorn van Veen TW(1996) Introduction: Ethnoveterinary research anddevelopment. In CM McCorkle, E Mathias, and Schillhorn van Veen TW (eds.): Ethnoveterinary Researchand Development. London: Intermediate Technology
Publications, pp. 1–24.
Matsuzawa T, and Yamakoshi G (1996) Comparison ofchimpanzee material culture between Bossou andNimba, West Africa. In AE Russon, KA Bard, and S
Taylor Parker (eds.): Reaching Into Thought. The
Minds of the Great Apes. Cambridge: University ofCambridge Press, pp. 211–232.
McCorkle CM, Mathias E, and Schillhorn van Veen TW(1996) Ethnoveterinary Research and Development.
London: Intermediate Technology Publications.
McGrew WC, Marchant L, and Nishida T (1996) Appendix: Great ape study sites. In Great Ape Societies.
Cambridge: Cambridge University Press.
McKey D (1978) Soil, vegetation and seed-eating by
black colobus monkeys. In GG Montgomery (ed.): The
Ecology of Arboreal Folivores. Washington, DC: Smithsonian Institute Press, pp. 423–437.
Messer EJ, and Wrangham RW (1995) In vitro testing of
the biological activity of Rubia cordifolia leaves on
primate Strongyloide species. Primates 37:105–108.
Milton K (1979) Factors in• u encing leaf choice byhowler monkeys: A test for some hypotheses of foodselection by generalist herbivores. Am. Nat. 114:362–
378.
Moore M (1979) Medicinal Plants of the Mountain West.
Santa Fe: The Museum of New Mexico Press.
Moutsamboté J, Yumoto T, Mitani M, Nishihara T,
Suzuki S, and Kuroda S (1994) Vegetation and list ofplant species identi• e d in the Nouabale´-Ndoki Forest,
Congo. TROPICS 3:277–293.
Müller K-H, Ahl C, and Hartman G (1997) Geophagy inmasked titi monkeys (Callicebus personatus melanochir). Primates 38:69–77.
Murakami A, Ohigashi H, and Koshimizu K (1994)
Possible anti-tumour promoting properties of tradi-̶ 288 ̶

Huffman]

EVIDENCE FOR SELF-MEDICATION

tional Thai foods and some of their active constituents. Asia Paci• c J. Clin. Nutr. 3:185–191.
Murakami A, Ohigashi H, and Koshimizu K (1996)
Anti-tumor promotion with food phytochemicals: A
strategy for cancer chemoprevention. Biosci. Biotech.
Biochem. 60:1–8.
Neuwinger HD (1996) African Ethnobotany: Chemistry,
Pharmacology, Toxicology. London: Chapman and Hill.
Newton PN, and Nishida T (1990) Possible buccal
administration of herbal drugs by wild chimpanzees,
Pan troglodytes. Anim. Behav. 39:798–801.
Nishida T (1987) Learning and cultural transmission in
non-human primates. In BB Smuts, DL Cheney, RM
Seyfarth, RW Wrangham, and TT Struhsaker (eds.):
Primate Societies. Chicago: The University of Chicago
Press, pp 462–474.
Nishida T, and Uehara S (1983) Natural diet of chimpanzees (Pan troglodytes schweinfurthii): Long term record from the Mahale Mountains, Tanzania. African
Studies Monographs 3:109–130.
Oates JF (1977) The guereza and its food. In TH
Clutton-Brock (ed.): Primate Ecology. London: Academic, pp. 276–321.
Oates JF (1978) Water-plant and soil consumption byguereza monkeys (Colobus guereza): A relationshipbetween minerals and toxins in the diet? Biotropica
10:241–253.
Oates JF, Swain T, and Zantovska J (1977) Secondary
compounds and food selection by colobus monkeys.
Biochem. Systems Ecol. 5:317–321.
Oates JF, Waterman PG, and Choo GM (1980) Food
selection by the south Indian leaf-monkey Presbytis
johnii, in relation to leaf chemistry. Oecologia 45:45–
56.
Ohigashi H (1995) Plants used medicinally by primatesin the wild and their physiologically active costituents. Report to the Minestry of Science, Education andCulture for 1994 Grant-in-Aid for Scienti• c Research(no. 06303012).
Ohigashi H, Jisaka M, Takagaki T, Nozaki H, Tada T,
Huffman MA, Nishida T, Kaji M, and Koshimizu K(1991) Bitter principle and a related steroid glucosidefrom Vernonia amygdalina, a possible medicinal plant
for wild chimpanzees. Agricultural Biol. Chem. 55:
1201–1203.
Ohigashi H, Sakai Y, Yamaguchi K, Umezaki I, andKoshimizu K (1992) Possible anti-tumor promoting
properties of marine algae and in vitro activity ofwakame seaweed extract. Biosci. Biotech. Biochem.
56:994–995.
Ohigashi H, Huffman MA, Izutsu D, Koshimizu K,
Kawanaka M, Sugiyama H, Kirby GC, Warhurst DC,
Allen D, Wright CW, Phillipson JD, Timmon-David P,
Delnas F, Elias R, and Balansard G (1994) Toward thechemical ecology of medicinal plant-use in chimpanzees: The case of Vernonia amygdalina Del. A plantused by wild chimpanzees possibly for parasiterelated diseases. J. Chem. Ecol. 20:541–553.
Okunji CO, and Iwu MM (1988) Control of schistomsomiasis using Nigerian medicinal molluscicides. Int. J.
Crude Drug Res. 26:246–252.
Oppenheimer JR (1968) Behavior and ecology of thewhite-faced monkey Cebus capucinus, on Barro Colorado Island, CZ, PhD thesis, University of Illinois,
Urbana, Ann Arbor: University Micro• • m s.
Page JE, Balza FF, Nishida T, and Towers GHN (1992)
Biologically active diterpenes from Aspilia mossambicensis, a chimpanzee medicinal plant. Phytochemistry31(10):3437–3439.
Page JE, Huffman MA, Smith V, and Towers GHN(1997) Chemical basis for medicinal consumption of
Aspilia leaves by chimpanzees: A re-analysis. J. Chem.
Ecol. 23:2211–2225.

199

Polderman AM, Krepel S, Baeta S, Blotkamp J, andGigase P (1991) Oesophagtostomiasis, a common infection of man in northern Togo and Ghana. Am. J. Trop.
Med. Hygiene 44:336–344.
Ponce-Monter H, Giron H, Lozoya X, Enriquez RG,
Bejar E, Estrada AV, and Gallegos AJ (1983) The
zoapatle III-biological anduterotonic properties ofaqueous plant extract. Contraception 27:239–253.
Price PW (1980) Evolutionary Biology of Parasitism.
Princeton, NJ: Princeton University Press.
Rausch R (1954) Studies on the heminth fauna of
Alaska. XXI. Taxonomy, morphological variation, andecology of Diphyllobothrium ursi n. sp. provis. on
Kodiak Island. J. Parasitol. 40:540–563.
Rausch R (1961) Notes on the black bear, Ursus americanus Pallas, in Alaska, with particular reference todentition and growth. Z. Saugetierk 26:77–107.
Revusky S (1984) Associative predispositions. In P Marler and HS Terrace (eds.): The Biology Learning.
Berlin: Springer-Verlag, pp. 447–460.
Richard A (1970) A comparative study of the activity
patterns and behavior of Aloutta villosa and Ateles
geoffroyi. Folia Primatol. 12:241–263.
Rodriguez E, Aregullin M, Nishida T, Uehara S, Wrangham RW, Abramowski Z, Finlayson A, and Towers
GHN (1985) Thiarubrin A, a bioactive constituent of
Aspilia (Asteraceae) consumed by wild chimpanzees.
Experientia 41:419–420.
Rodriguez E, and Wrangham RW (1993) Zoopharmacognosy: The use of medicinal plants by animals. In KR
Downum, JT Romeo, and H Stafford (eds.): Recent
Advances in Phytochemistry, vol. 27: Phytochemical
Potential of Tropic Plants. New York: Plenum, pp.
89–105.
Roepstorff A, Bjørn H, and Nansen P (1987) Resistenceof Oesophagostomum spp. in pigs to pyrantel citrate.
Vet. Parasitol. 24:229–239.
Sadlier RM (1969) The Ecology of Reproduction in Wild
and Domestic Mammals. London: Methuer.
Salafsky B, Wang Y-S, Kevin MB, Hill H, and Fusco AC(1984) The role of prostaglandins in cercarial (Schistosoma mansoni) response to free fatty acids. J. Parasitol. 70:584–591.
Sarmiento EE, Butynski TM, and Kalina J (1996)
Gorillas of Bwindi-Impenetrable Forest and theVirunga Volcanoes: Taxonomic implications of morphological and ecological differences. Am. J. Primatol.
40:1–21.
Sayer JA, Harcourt CS, and Collins NM (1992) The
Conservation Atlas of Tropical Forests, Africa. New
York, IUCN.
Shiba T (1976) Chemistry of bitter and hot taste.
Kagaku Sosetsu 14:129–156.
Smolenski SJ, Silinis H, and Farnsworth NR (1974)
Alkaloid screening. V. Lloydia 37:506–536.
Starker LA (1976) Phytooestrogens: Adverse effects on
reproduction in California quail. Science 191:98–100.
Struhsaker TT (1997) Ecology of an African Rain Forest.
Gainesville: University Press of Florida.
Sugiyama Y, and Koman J (1992) The • ora of Bossou: Itsutilization by chimpanzees and humans. African Studies Monographs 13:127–169.
Sukhdeo MVM, and Sukhdeo SC (1994) Optimal habitat
selection behaviour by helminths within the host.
Parasitology 109:41–55.
Synott TJ (1985) A checklist of the • o ra of Budongo
Forest Reserve, Uganda, with notes on ecology andphenology. CFI Occasional Papers No. 27, Department of Forestry Commonwealth Forestry Institute,
Oxford, University of Oxford.
Takasaki H, and Hunt K (1987) Further medicinal plant
consumption in wild chimpanzees? African Studies
Monographs 8:125–128.

̶ 289 ̶200

YEARBOOK OF PHYSICAL ANTHROPOLOGY

Toft CA, Aeschlimann A, and Bolis L (1991) ParasiteHost Associations; Coexistence or Con• ict? Oxford:
Oxford Science Publications.
Toubiana R, and Gaudemer A (1967) Structure duvernolide, nouvel ester sesquiterpique isole de Vernonia colorata. Tetrahedron Lett. 14:1333–1336.
Towers GHN, Abramowski Z, Finlayson AJ, and Zucconi
A (1985) Antibiotic properties of thiarubrine-A, anaturally occurring dithiacyclohedadiene polyine.
Planta Medica 3:225–229.
Tutin CEG, White LJT, Williamson EA, Fernandez M,
and McPherson G (1994) List of plant species identi• ed in the northern part of the Lope´ Reserve, Gabon.
TROPICS 3:249–276.
Vermeer J (1995) A garden of enrichment. Animal
Keepers’ Forum 5:165–167.
Wallis J (1992) Socioenvironmental effects on timing of• rst postpartum cycles in chimpanzees. In T Nishida,
WC McGrew, P Marler, M Pickford, and F de Waal
(eds.): Topics in Primatology, Vol. 1: Human Origins.
Tokyo: University of Tokyo Press, pp. 119–130.
Wallis J (1994) Socioenvironmental effects on full anogenital swellings in adolescent female chimpanzees.
In JJ Roeder, B Thierry, JR Anderson, and N Herrenschmidt (eds.): Current Primatology, Vol. 2: Social
Development, Learning and Behavior. Strasbourg:
University of Louis Pasteur, pp. 25–32.
Wallis J (1995) Seasonal in• uen ce on reproduction inchimpanzees of Gombe National Park. Int. J. Primatol. 16:435–451.
Wallis J (1997) A survey of reproductive parameters in
the free-ranging chimpanzees of Gombe National
Park. J. Reprod. Fertil. 109:297–307.
Waterman PG (1984) Food acquisition and processing asa function of plant chemistry. In DJ Chivers, BA Wood,and A Bilsborough (eds.): Food Acquisition and Processing in Primates. New York: Plenum, pp. 177–211.
Watt JM, and Breyer-Brandwijk MG (1962) The Medicinal and Poisonous Plants of Southern and East Africa.
Edinburgh: E. and S. Livingstone.
Westley J (1980) Rhodanese and the sulfane pool. In WB
Jakoby (ed.): Enzymatic basis of detoxi• cation. vol. 2.
New York: Academic, pp. 245–262.
Whitten PL (1983) Flowers, fertility and females. Abstract. Am. J. Phys. Anthropol. 60:269–270.

[Vol. 40, 1997

Wink M, Hofer A, Bil• n ger M, Englert E, Martin M, andSchneider D (1993) Geese and dietary allelochemicals—food palatability and geophagy. Chemoecology
4:93–107.
Wrangham RW (1977) Feeding behavior of chimpanzees
in Gombe National Park, Tanzania. In TH CluttonBrock (ed.): Primate Ecology. London: Academic, pp.
504–538.
Wrangham RW (1995) Relationship of chimpanzee leafswallowing to a tapeworm infection. Am. J. Phys.
Primatol. 37:297–303.
Wrangham RW, and Goodall J (1989) Chimpanzee use of
medicinal leaves. In PG Heltne and LA Marquardt(eds.): Understanding Chimpanzees. Cambridge, MA:
Harvard University Press, pp. 22–37.
Wrangham RW, and Nishida T (1983) Aspilia spp.
leaves: A puzzle in the feeding behavior of wild
chimpanzees. Primates 24:276–282.
Wrangham RW, and Waterman PG (1981) Condensed
tannins in fruits eaten by chimpanzees. Biotropica
15:217–222.
Wrangham RW, Rogers ME, and Isabirye-Basuta G(1993) Ape food density in the ground layer in Kibale
Forest, Uganda. African J. Ecol. 31:49–57.
Wright C, Phillipson GC, Kirby DV, Huffman MA, andOhigashi H (1993) Do chimpanzees know how to treat
protozoal diseases? Paper presentation at the Fifth
British Society for Parasitology Malaria Meeting,
September, 1993: Oxford.
Yumoto T, Yamagiwa J, Mwanza N, and Maruhashi T(1994) List of plant species identi• ed in Kahuzi-Biega
National Park, Zaire. TROPICS 3:295–308.
Zahorik DM (1977) Associative and non-associative factors in learned food preferences. In LM Barker, MR
Best, and M Domjan (eds.): Learning Mechanisms inFood Selection. Baylor, TX: Baylor University Press,
pp. 181–199.
Zahorik DM, and Albro Houpt K (1977) The concept ofnutritional wisdom: Applicability of laboratory learning models to large herbivores. In LM Barker, MR
Best, and M Domjan (eds.): Learning Mechanisms inFood Selection. Baylor, TX: Baylor University Press,
pp. 45–67.

̶ 290 ̶̶ 291 ̶̶ 292 ̶̶ 293 ̶̶ 294 ̶̶ 295 ̶̶ 296 ̶̶ 297 ̶̶ 298 ̶̶ 299 ̶̶ 300 ̶̶ 301 ̶̶ 302 ̶̶ 303 ̶