Cyanogenic Bamboo by a Newly
KENNETH E. GLANDER', PATRICIA
Biological Anthropology and Anatomy, Duke Uniuersity, Durham, North
Biology, California Institute
Plant Biology, Uniuersity of Illinois, Urbana; 'Parc Botanique et Zoologique
Tsinibazaza, Antananariuo, Democratic Republic
Three species of bamboo-eating lemurs were found to be sympatric in the
southeastern rain forests of Madagascar. Sympatric species generally dif-
fer in habitat utilization or diet, but these three closely related bamboo
lemurs lived in the same habitat and all ate bamboo. Behavioral observa-
tion revealed that they did select different parts of the bamboo, and chem-
ical analyses confirmed that there was a difference in the secondary
compound content present in those selections. The growing tips of
selected by the golden bamboo lemur
contained 15 mg of cyanide per 100 g fresh weight bamboo while
the leaves of
selected by the gentle bamboo lemur
and the mature culms of
selected by the greater bamboo
did not contain cyanide. Since each individual golden
bamboo lemur ate about
of bamboo per day, they daily ingested
about 12 times the lethal dose of cyanide. The mechanism by which this
small primate avoids the acute and chronic symptoms of cyanide poision-
ing is unknown.
Hapalemur aureus, Hapalemur griseus, Hapalemur simus,
In 1986, while studying the gentle bamboo lemur
Ranomafana National Park, Madagascar, Wright and colleagues [Wright
1987; Meier et al., 19871 discovered a new species of bamboo lemur
golden bamboo lemur) and found another species that had not been seen since the
or greater bamboo lemur). All three of these lemurs live in
the same habitat and all three eat bamboo, in the case of the golden and greater
bamboo lemur, the same species of bamboo [Wright et
19871. Here we report the
preliminary results of an ongoing behavioral and ecological study of these three
Received for publication February
revision accepted August
Address reprint requests to K.E. Glander, Department
Biological Anthropology and Anatomy,
Duke University, Durham, NC
MATERIALS AND METHODS
Golden bamboo lemurs were observed for a total of 153 hours during June-
August 1986; June-November 1987; and June-November 1988. Marked individ-
uals were followed for as long as they could be kept in sight. Activities were
recorded, and if the activity was feeding, the part of the plant eaten was noted.
individuals was accomplished in May 1988
using the Pneu-dart system (Pneu-Dart Inc.,
Williamsport, PA 17701). This
system employs disposable non-barbed darts with a 318-inch needle delivered by a
carbon dioxide powered gun. The darts were loaded with
mg) of Ketalar
(Ketamine hydrochloride, 100 mglml) (Bristol Laboratories, Syracuse, NY 13201).
Samples of two species of bamboo,
were collected and tested in May 1987; May, June, and December
1988; and May 1989. The four parts of each plant collected were the leaf, new shoot,
young stem pith, and trunk. Collections
made at the exact location where
individuals were feeding or the material dropped was collected in an effort to
obtain plant material as similar as possible to what the animals ate.
The bamboo genus
occurs in Indomalaysia and Madagascar
[Airy Shaw, 19731. Both
species in this study are native to this
area of Madagascar and there are at least 10 species of bamboo in the park area
(Edelman personal communication). This group of grasses is poorly known and the
systematic status of these two species and the genus
Thus the identification of the bamboo in this paper as
must be consid-
The presence or absence of cyanide was determined by the Feigl Anger test
Anger, 1966; Tantisewie et al., 19691. All analyses were started and
completed in the shade, at the same temperature and humidity. All tests were done
in the field in May 1987; May, June, and December 1988; and May 1989. The plant
parts tested were chopped into 1-cm-long bits and added to glass test tubes. The
material was macerated in the bottom of vials before a strip of filter paper im-
pregnated with Feigl Anger solution [Feigl
Anger, 19661 was added and a cork
placed in the top of the vials. Care was taken
that the paper did not touch the
plant material. The white strip changed to blue in the presence of cyanide. The
color of the test strips was noted at intervals of 15, 30, 60, and 240 minutes.
Replicates (a minimum of 3-4 from each plant) of leaves, young stems, and mature
stems of each species were examined.
To determine the amount of cyanide present, the outer fibrous material of the
bamboo was removed from approximately the last foot of growth collected on May
20, 1987. The white tender inner material (115 g) was cut into small pieces as
quickly as possible and added to the hot alcoholic extraction medium (Saint
Claude, Rhum de Luxe, Extra Fin, Special 43", Carte Noire). The mixture was
boiled for 10 minutes, cooled, and decanted. After boiling, the residual plant ma-
terial still contained residual cyanogenic materials as indicated by tests with Feigl
Anger paper [Tantisewie et al., 1969; Feigl
Anger, 19661. This material was
reboiled with 200 ml water for an additional 10 minutes. It still gave positive tests
Lemur Niche Separation
for cyanide, and it is clear that the extraction under field conditions was ineffi-
cient. The percent of cyanide was later determined in the laboratory.
Cyanogenic compounds in the extract were decomposed by addition of emulsin
Louis, MO) and the resulting cyanide was captured in 0.1 N sodium
hydroxide solution in Warburg flasks. The basic solution was removed and cyanide
content determined by colorimetric analysis [Lambert et al., 19751. Each sample
was repeated four times. A control was run on the extraction medium (Rhum de
At least five species of bamboo are common at the research site. One of these,
was the principal food
golden bamboo lemurs and the only bamboo
species they were observed to eat. They ate shoots, leaf bases, pith, and the viny
part of this bamboo. Greater bamboo lemurs ate the mature culms (stalks) of the
same bamboo species while gentle bamboo lemurs ate the leaf bases and blades of
a related species of bamboo,
Ninety-one percent of the golden bamboo lemurs’ feeding minutes were spent
eating bamboo, while the remainder was spent feeding on one unknown palm fruit
and one unknown
fruit. Feeding began shortly after dawn (0530) and
continued for an average of
45, range 20-50). These feeding bouts
were followed by rest periods of 30 to
minutes, which were followed by another
feeding bout and rest period. Feeding and resting alternated until an extended
period began at 1000 and lasted until 1500. After 1500, feeding and resting periods
continued to alternate until dark at 1745.
From June to August, bamboo shoots are rare and the golden bamboo lemurs
their feeding time eating leaf bases and the inside of the viny part of
December, new shoots of
were again common, and
the golden bamboo lemurs spent
of their feeding time eating shoots with the
remainder spent eating bamboo leaf bases and the pith from the viny part of
as well as the palm and
The shoots, leaf bases, and pith of
all contained cyanide, with the
pith containing high levels. Each of the more than 200 samples tested turned the
test paper dark blue within the first 30 seconds. Leaf blades and culms of
tested negative for cyanide as did all plant parts of
various times during a three-year period (see Collection of Plant Material) indi-
cated no seasonal variation in the production of cyanide.
The cyanide content of the extracted sample was 15 mg HCN per 100 g fresh
weight. The extraction medium (Rhum de Luxe) contained no cyanide.
The only wild-caught
weighed 770 g, whereas the average weight of
the Duke Primate Center was 936 g (Table
average weight of three
captured during May 1987 was 1,560 g (Table
One of the adult males was captured again in October 1988 and had gained 120
The only weight for adult
is 2,365 g for one adult male [Meier et al.,
Plants that release more than 10-20 mg HCN per 100 g of fresh plant tissue
are considered potentially dangerous to livestock [Moran, 1954; Kingsbury, 19641.
Therefore, the amount of cyanide
mgilO0 g fresh weight) found in the soft
"Captive animals held at the Duke Primate Center.
hSame individual captured in
stems and growing tips of
would be dangerous to most mammals, but
was not harmful to the golden bamboo lemurs.
Free hydrogen cyanide is readily absorbed by most animals and is highly toxic
[Poulton, 19831. An oral lethal dose of HCN for the mouse is 3.7 mgikg; dog,
mgikg; cat, 2.0 mgikg; rat,
Fairchild, 19761. The lethal
dose for sheep is 2.0 mgikg body weight [Harborne, 19821. The oral lethal dose of
hydrogen cyanide for humans is 0.5-3.5 mgikg body weight or about 50-250 mg
for a typical adult human [Montgomery, 1969; Christensen
Assuming that an adult golden bamboo lemur
kg) is proportionately as
sensitive to cyanide as the animals above, an average (excluding humans) lethal
dose of 6.5 mg would be found in
g of bamboo eaten. The golden bamboo lemurs
g of bamboo per day, or about 12 times the lethal dosage of cyanide
daily. This undoubtedly represents a low estimate because of the inefficiency of the
field extraction method. Much larger amounts of cyanide (90-800 mg HCN per
g fresh weight) have been reported from other bamboo species
We do not know how golden bamboo lemurs avoid cyanide poisoning, but there
several possibilities. For most animals, the major mechanism of cyanide detox-
ification involves conversion of cyanide to thiocyanate [Montgomery, 1979
process requires the enzyme rhodanese, which is present in most animal tissues,
plus amino acids such as methionine or cysteine to convert cyanide to thiocyanate.
Based on nutritional data for other bamboo species, sulfur-containing amino acids
are relatively low ISchaller et al., 19851. Thus, this method of detoxification seems
unlikely for the golden bamboo lemur.
Another method of detoxification is to keep the stomach acidic, since the
lease of cyanide is inhibited by low pH. For humans and other monogastric ani-
mals, acidic stomach conditions prevent the formation of cyanide, Both the greater
bamboo lemur (which eats mature culms) and the gentle bamboo lemur (which eats
leaf bases) have unspecialized stomachs [Hill, 1953
and short, globular ceca that
lack apical narrowing and are the simplest of all the lemurs [Tattersall, 19821. This
simplicity in their stomachs and ceca is surprising given their extremely fibrous
diet, but resembles the digestive system of the panda [Schaller et al., 19851. The
digestive system of the golden bamboo lemur is unstudied.
plentiful resource, but relatively few mammals and certainly no
other prosimians utilize it for food. Probably the best-known herbivore that feeds
almost exclusively on bamboo is the giant panda
[Schaller et al., 19851. During some portions of the year, the giant panda eats
shoots of the genus
an exclusive food, but not those of the genus
which is common in the same area [Schaller et al., 19851. These
shoots have considerable total fiber (76-90%? and are low in nutrients, especially
the sulfur-containing amino acid methionine [Schaller
al., 1985; Dierenfeld et
al., 1982; Dierenfeld,
but apparently were not tested for cyanide.
Other mammals utilizing this abundant food resource are two Southeast Asian
a South American rat
and African monkey
(Cercopithecus mitus kanditi),
South American monkey
[Emmons, 1981; Schaller et al., 1985;
The gentle bamboo lemur
can be found throughout most of the
eastern rain forest, but the golden bamboo lemur
is among the rarest
primates of Madagascar and only found in the southeastern rainforest. Golden
bamboo lemurs’ geographical distribution is closely linked to that of bamboo and
may be limited to those areas of Madagascar where cyanogenic bamboo occurs.
The panda-like bamboo lemurs have exploited an open niche and appear to
have specialized to the extent of dividing up the niche based on the chemical and
nutrient content of the bamboo. Niche partitioning at this level may be more
common among primates than has been formerly appreciated. Ganzhorn [1988
suggested that food selection based on primary and secondary plant chemicals is an
important factor in the mechanisms permitting several primate species to be sym-
patric. Additional studies of the three bamboo-eating lemurs of Madagascar are
presently underway to further define this dynamic plant-primate interaction.
as a principal component of their diet.
Three species of bamboo-eating lemurs are sympatric in the rain forests of
2) These three species of lemurs utilize the same habitat, and all eat bamboo
The three species select different parts of the bamboo.
The diet of the golden bamboo lemur contained at least 15 mg of cyanide per
Based on a daily diet of
g of bamboo, the golden bamboo lemur ingested
6) The mechanism by which the golden bamboo lemurs avoid cyanide poison-
100 grams of fresh weight bamboo.
about 12 times the lethal dose of cyanide each day.
ing is unknown.
This study was supported by the Sub-Saharan African Cooperative Science
Program of the National Science Foundation (NSF INT-86022861, Wildlife Con-
servation International, World Wildlife Fund-US Primate Program, Duke Uni-
versity Research Council, National Geographic Society, Chicago Zoological Soci-
ety, and the Dourocouli Foundation. We thank the Ministere de la Production
des Eaux et Fortits, Department of Water and
Forests of Madagascar, and the Missouri Botanical Garden for their cooperation
and help. Thanks to George Schatz, Porter Lowry
Roan McNab, Anita Brinker,
David Meyers, Patrick Daniels, Joe Macedonia, and our guides, Emile Rajery,
Loret Rasabo, and Pierre Talata of Ambatolahy without whose assistance the
successful completion of this study would have been difficult. Our special thanks to
Tom Soderstrom, David Edelman, and Emmet Judziewicz for identifying the bam-
boo. This is paper no.
from the Duke University Primate Center.
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