One Reserve, Three Primates: Applying a Holistic
Approach to Understand the Interconnections Among Ring-tailed
Lemurs (Lemur catta), Verreaux's
Sifaka (Propithecus verreauxi),
and Humans (Homo sapiens) at
Beza Mahafaly Special Reserve, Madagascar.
James E. Loudon 1*, Michelle L. Sauther 1,
Krista D. Fish 1, Mandala Hunter-Ishikawa 2,
Youssouf Jacky Ibrahim 3
Abstract: We applied
cultural anthropological, ethological, and parasitological
methodologies to investigate the interplay among three
primate species, ring-tailed lemurs (Lemur catta), Verreaux's
sifaka (Propithecus verreauxi), and humans (Homo
sapiens) who live within the same habitat (i.e. in
sympatry) around the Beza Mahafaly Special Reserve, Madagascar.
Through a fusion of these methodologies we hope to provide
a holistic understanding of the advantages and disadvantages
of human-nonhuman primate sympatry. Interviews and questionnaires
provided us with initial insights regarding the local peoples'
attitudes toward sympatric strepsirrhine primates. Origin
myths indicate a close association between humans, ring-tailed
lemurs, and Verreaux's sifaka, which may serve as an important
basis for positive conservation perspectives among the local
people. These include lemur hunting taboos and special ancestral
forests that are protected against deforestation. However,
paleontological data indicate that these cultural perceptions
may be of recent origin.
Close human-nonhuman primate associations
can also have negative effects. We found that some nonhuman
primate behavioral activities appear associated with increasing
parasite loads, and may act as potential avenues of parasite
transmission. Fecal analyses revealed that groups of ring-tailed
lemurs that frequented the camp, and interact on a regular
basis with humans harbor more endoparasites. These lemur
“camp” groups engaged in coprophagy (fecal ingestion) of
human, dog (Canis familiaris), and zebu (Bos indicus)
fecal matter. In contrast, analyses of Verreaux's sifaka
fecal matter revealed no parasites. Verreaux's sifaka were
rarely terrestrial, generally avoided humans, and were not
observed engaging in coprophagy. This suggests that each
strepsirrhines species' behavioral patterns and socioecology
directly affect its likelihood of acquiring parasitic infections,
and this is currently being studied in more depth at the
We feel that incorporating local people into conservation
initiatives are vital for success. This requires an understanding
of human-nonhuman primate interconnections, the perspective
of local peoples regarding their surroundings, knowledge
of nonhuman primate behavior, and epidemiological factors.
Keywords: ethnoprimatology, ring-tailed
lemurs, Verreaux's sifaka
1Department of Anthropology, University of Colorado-Boulder
Boulder, CO USA 80309-0233
2 Colorado State University College of Vet Med
and Biomedical Sciences
3 Département de Sciences Biologie, Université d'
Toliara, Toliara, Madagascar
In many regions throughout the world where nonhuman primates
naturally occur, their lives are interconnected with humans.
These interconnections are the product of a broad spectrum
of scenarios such as pet ownership (Jones-Engel et al. 2001;
Duarte-Quiroga and Estrada 2003), logging (Chapman et al.
2000), hunting (Alvard et al. 1997; Workman 2004), crop raiding
(Naughton-Treves et al. 1998), ecotourism (Fuentes and Wolfe
2002), and field-based studies by human researchers (Jones-Engel
et al. 2003). As human populations grow the likelihood of
human-nonhuman encounters increases. In such circumstances,
humans and nonhuman primates may partially or completely
overlap and ultimately compete for contested resources, including
space as well as crops. Conflicts arising from contested
resources between these primates often result in the poaching
or killing of nonhuman primates (Wolfe et al. 1998). In addition,
increased human-primate contact can act as an avenue for
bi-directional zoonotic transmission (Jones-Engel et al.
The goal of ethnoprimatology is to study the interactions
of humans and nonhuman primates, which live in sympatric
associations (Sponsel et al. 2002) by employing cultural
anthropological and primatological methodologies (Sponsel
1997). It has long been noted that nonhuman primates have
been considered sacred, abhorred, or both, by their human
counterparts. These attitudes are influenced by traditional
(Wheatley 1999; Wheatley et al.. 2002; Cormier 2002; Sicotte
and Uwengeli 2002) and religious (Carter and Carter 1999;
Burton 2002; Wolfe 2002) components of human societies, nonhuman
primate behaviors (Naughton-Treves et al. 1998), and the
context or social atmosphere of the human society (Loudon
et al. in press). Thus a fusion of traditional anthropological
methods (i.e. ethnoprimatology) affords the ethnographer
or primatologist with the appropriate toolkit to fully understand
human-nonhuman primate interactions and simultaneously provides
insights into the behavior of both humans and their nonhuman
Madagascar is an excellent locality to study the historical
and present-day interplay between humans and nonhuman primates.
Humans only inhabited the island as recently as 2000 years
ago and subsequently 1/3 of all lemur species went extinct
(Ganzhorn et al. 1999). Today, large regions of Madagascar
have been denuded of their forests and natural habitat (Sussman
1999). Although many reserves exist, considerable anthropogenic
change has occurred outside of such areas. One such reserve
is the Beza Mahafaly Special Reserve (BMSR) in southwestern
Madagascar. What is intriguing about BMSR is its success.
This reserve has remained primarily intact, without human
influence for over twenty years, whereas areas around the
reserve have been fragmented and degraded by the local Mahafaly
(Whitelaw et al. 2005). To date, several primatologists tackle
conservation initiatives from the perspective of “how” and
“why” national parks, reserves, or protected areas fail.
In contrast, we were interested in the “how” and “why” this
reserve is successful (Ratsirarson 2003).
Ring-tailed lemur, Lemur catta within parcel
1 of the Beza Mahafaly Special Reserve.
critical aspect of ethnoprimatological investigations is
the behavior of the nonhuman primates and the ramifications
of such behavior. Here, we focus on two nonhuman primates,
the ring-tailed lemur (Lemur catta) (figure 1)
and Verreaux's sifaka (Propithecus verreauxi)
(figure 2). These strepsrrhines are found in sympatric associations
throughout southern Madagascar. While the two species share
a common ancestry, as do all extant lemurs (Karanth et al.,
2005), they differ in both behavior and morphology (Tattersall,
1982). Ring-tailed lemurs can be characterized as dietary
generalists consuming a wide spectrum of foods including
stems, fruits, flowers, and invertebrates based on the seasonal
availability of each (Sauther et al.. 1999; Jolly 2003).
Furthermore L. catta occupy all levels of the forest
canopy and is the most terrestrial of the Malagasy strepsirrhines
(Fleagle 1999). In contrast, sifaka are primarily arboreal,
use the terrestrial substrate more infrequently, and are
predominantly folivorous (Richard et al. 1993).
Figure 2. Verreaux's sifaka, Propithecus
verreauxi verreauxi within parcel 1 of the Beza
Mahafaly Special Reserve.
both species live sympatrically, yet exhibit distinct behavioral
repertoires allowing for excellent comparisons between
their socioecology and parasite ecology. In this paper we
present preliminary, descriptive results of an on-going long-term
project, which is currently investigating the socioecology
and parasite ecology of both of these species at the BMSR.
The long-term project has four goals: to examine how each
species' socioecology affects parasite type and prevalence,
including seasonal fluctuations of parasites among each
primate species; to examine the behaviors that ring-tailed
lemurs and Verreaux's sifaka utilize to potentially eliminate,
avoid, or reduce parasite infections; to determine how social
rank and sex affects individual parasite prevalence for both
species; and to understand how an anthropogenically-altered
habitat affects all of these patterns as compared to those
documented for groups living in undisturbed habitats. This
project integrates primatological, cultural anthropological,
and parasitological methodologies to understand how the attitudes
of Mahafaly toward the reserve as well as the interactions
between nonhuman primates and the Mahafaly impact the success
Study Site and Subjects. Research
was conducted at BMSR (23º30'S latitude,
44º40'E longitude) in southwestern Madagascar during
a six-week period in the summer of 2004. In 1978 the local
people of Firaisana
(district) of Beavoha officially granted the two parcels
to ESSA/Forêts, Universitê d'Antananarivo (Ratsirarson
2003). This reserve integrated conservation and development
from the start. The local community requested and received
canal irrigation, road improvements, a new school and new
wells all of which were provided through support from WWF
(World Wildlife Fund) and USAID (United States Agency for
International Development) (Ratsirarson 2003). BMSR became
a special government reserve in 1986 (Sussman 1991; Ratsirarson
2003) and is now coordinated by the National
Association for the Management of Protected Areas (ANGAP).
The reserve and surrounding areas is characterized by distinct
wet (October-April) and dry seasons (May-August),
and periodically experiences droughts (e.g., Sauther 1991,
1993, 1999; Gould et al. 1999; Ratsirarson
2003 ). The habitat is highly seasonal with approximately
99% of the annual rainfall occurring during the wet season
(Sauther 1999). While this study focused on the socioecology
of ring-tailed lemurs and Verreaux's sifaka, nocturnal white-footed
sportive lemurs (Lepilemur leucopus), gray mouse
lemurs (Microcebus murinus), and gray brown mouse
lemurs (Microcebus griseorufus) also inhabit the
reserve (Ratsirarson 2003).
The local people are composed of Mahafaly,
Antandroy and Tanala peoples (figure 3), (Ratsirarson
2003). Families live in straw and wood huts, with most
family members coming from the surrounding areas. This is
a patriarchal, agrarian society that focuses on maize, cassava
and sweet potatoes (bageda), as well as zebu cattle,
goats, sheep and chickens. Two types of herding methods are
used. Midada allows livestock to roam freely in
the forest with the owner gathering periodically. The other, miarakandrovy involve
active herding of the animals with livestock kept near the
village each evening (Ratsirarson 2003). Land
is viewed as privately owned and inherited from ancestors.
Tortoises and lemurs are fady (taboo) to hunt (Rambeloson
3. Local Mahafaly people
near Beza Mahafaly Special Reserve.
BMSR consists of a campsite and two parcels
of forests (Ratsirarson 2003). Parcel 1 is approximately
80 ha and is protected against accidental grazing by sheep,
goats, and cattle via a barbed wire fence. This parcel is
a riparian forest patch that is located on the Sakamena River,
dominated by kily trees (Tamarindus indica) and
exhibits a high forest canopy with a rich understory of saplings,
lianas, and terrestrial herbs (Sauther 1991). Parcel 2 is
approximately 500 ha, is not protected by a fence, and is
used by the local people from the neighboring villages for
grazing livestock. Parcel 2 is open and dry, and is characterized
by xerophytic vegetation (Ratsirarson 2003). At the time
of this research the camp consisted of a small administrative
building for the ANGAP officials, a small museum, a pit latrine
for visitors and researchers, an open-air latrine used by
the local Mahafaly people (the use of pit latrines is fady),
and several mud block structures for the on-site families
(figure 4). During this study two families lived at the site
throughout the year.
These families cultivated maize and manioc in nearby fields,
and raised chickens, ducks, and turkeys all of which ranged
primarily within the camp area and surrounding forest. Some
social groups of ring-tailed lemurs and sifaka utilize both
the reserve and camp. Most sifaka and ring-tailed lemurs
in this population bear color-coded collars that identify
their group, and a tag number that identifies each individual
(Figure 2). The ring-tailed lemurs and sifaka at BMSR has
been the subject of a number of long-term studies by Drs.
Robert Sussman, Alison Richard, Diane Brockman, Michelle
Sauther and Lisa Gould.
4. Villagers home in the
camp near parcel 1 of the Beza Mahafaly Special Reserve.
Note ring-tailed lemurs on the roof.
Behavioral sampling. Each
species was intensively followed for four hours per day for
six weeks. Species followed were rotated daily. Thus, each
lemur species was sampled for a total of eight-four hours.
Average group size of ring-tailed lemur groups was 15 individuals
while the average size of sifaka groups was 6. Sample size
was n = 30 for the ring-tailed lemurs and n = 20 for the
sifaka. We used scan sampling (Altmann 1974) to collect behavioral
data on ring-tailed lemurs and sifaka. Sampled behaviors
are listed in Tables 1 and 2. All-occurrence sampling (Altmann
1974) was employed to examine the context and duration of
interactions between humans and nonhuman primates. A “human-nonhuman
primate interaction” was defined as a behavioral interaction
between the two species that exceeded 10 seconds and included
such behaviors as lemurs or humans approaching one another,
humans feeding the lemurs and chasing them from a human food
resource (Figures 4 and 5). Glances and visual monitoring
between species were not considered an “interaction.” Both
methodologies were coupled with ad libitum sampling.
Table 1. Behaviors ring-tailed lemurs engaged in
that reduce, avoid, eliminate, or increase the likelihood
of obtaining certain parasitic infections at Beza Mahafaly.
Autogroom (groom self)
Allogroom (groom others)
Avoid Feces/Latrine Behavior1
Coprophagy (fecal ingestion)
Consumption of medicinal
foods (e.g. foods high in tannins).
Consumption from human
Geophagy (soil eating)
1Latrine behavior refers to the whole troop tending to
defecate within the same area and sometimes even near the
same spot. By doing so, the lemurs may avoid their own and
other group's feces.
Table 2. Behaviors Verreaux's sifaka engaged in
that reduce, avoid, eliminate, or increase the likelihood
of obtaining certain parasitic infections at Beza Mahafaly.
Autogroom (groom self)
Allogroom (groom others)
Consumption of medicinal
foods (e.g. foods high in tannins).
Geophagy (soil eating)
Parasitological protocols. Ring-tailed
lemurs were captured using a Telinject blow dart system and
the drug mixture of Ketamine and Diazepam, as part of the
long-term investigation of this population's health profiles
(Sauther et al., in press). We used protocols developed over
the past 17 years and 360 captures at Beza Mahafaly (see
Sauther et al. in press for a complete description). After
examination and the collection of biological samples, individuals
were released in the area where originally captured (normally
within six hours). We followed all IACUC guidelines for these
captures. Fecal samples were collected either as voided by
lemurs under anesthesia or during lemur behavioral follow.
All fecal samples were collected fresh. We examined the fecal
parasites of 70 ring-tailed lemurs and 18 Verreaux's sifaka.
Methods included fecal smears and fecal floatation methodologies.
Fecal smear techniques detect the presence of non-buoyant
and recently shed parasites within the animal's feces. Fecal
floatation was used for separating helminthes eggs, and protozoan
cysts from fecal matter. This allows for the identification
of buoyant endoparasites and eggs, which float to the top
of a cover slip (Ash and Oribel, 1987). We collected ectoparasites
from anesthetized ring-tailed lemurs by using a tick comb
for mites and tweezers to extract ticks.
5. Local villager feeding
a banana to a ring-tailed lemur within camp.
Interviews. We conducted questionnaires
(Benard 2000) and non-scripted interviews to examine the
local Mahafaly peoples' attitudes regarding ring-tailed lemurs
and sifaka and the local folklores and origin myths surrounding
each nonhuman primate (see Box 1 for an example of these
questions). All interviews were conducted in Mahafaly by
one of the authors, Mr. Jacky Yousouff, as well as a local
assistant, Mr. Emady Rigobert. Thus interviewers were well
known to the local people. Interviews took place at the villages
of Analafaly, Ambinda, and Manasoa. Each interview was conducted
with elder men or the village president (all older, male
individuals). Thus our interview data are biased toward male
perspectives of the reserve and the strepsirrhines inhabiting
it. This was due to local traditions of the kabary (Malagasy
word meaning "public discussion" similar to a public
hearing.). No compensation was provided to avoid influencing
Box 1. Interview Questions
Is the Beza Mahafaly Reserve
good? What benefits do you derive from the reserve?
How did the reserve begin? What village owned the
land before it became a reserve?
Should animals graze in the reserve?
What is the future of the reserve?
What are your feelings regarding the researchers
that study at the reserve?
Are the ring-tailed lemurs (maky) and
sifaka sacred or special?
What is the origin of the maky and sifaka?
Do maky and sifaka raid crops? If so,
how do you prevent crop raiding?
Do people eat makyor sifaka?
How long do maky and sifaka live?
What are the differences between maky and
What do the maky and sifaka eat?
How many maky and sifaka live here?
Differences in Behavior. Preliminary data
indicate that ring-tailed lemurs and Verreaux's sifaka differ
in their socioecology and behavior in ways that may affect
each species' disease ecology. Ring-tailed lemurs are more
terrestrial and may thus encounter more potential avenues
of disease transmission than the less terrestrial sifaka.
In comparison to sifaka, ring-tailed lemurs at BMSR form
larger social groups and frequently interact with other social
groups increasing the potential for parasite transfer. There
were also a number of behaviors that both species engaged
in that could affect parasite type and prevalence. Both species
consumed food high in tannins (kily fruit [Tamarindus
indica]), (Sauther and Ganzhorn, unpublished data),
as well as dirt, and termite soil. Each morning, and throughout
the day, both species were observed sitting in sunlight in
a behavior known as “sunning” (Jolly 2003). Ring-tailed lemurs
preferentially used specific locations to defecate, as seen
in the use of "latrines" by other lemur species
(Erwin et al., 2004). Soiled locations were not used by ring-tailed
lemurs, other than to eliminate waste (Loudon, pers.obs).
6. Ring-tailed lemurs in
the camp near parcel 1 of the Beza Mahafaly Special
Reserve feeding on cattle forage.
Our preliminary observations also indicate that groups living
within human-altered habitats change their behavior in ways
that could affect their disease ecology. Local traditions
of the Mahafaly people of the BMSR area prohibit the use
of pit-latrines, instead using an open-air “toilet area.”
Ring-tailed lemur groups that commonly used the camp as part
of their home range were observed ingesting human feces from
this traditional toilet area. They also consumed zebu (Bos
taurus) and dog (Canis familiaris) feces
occasionally. Each age and sex class was observed consuming
feces. Interestingly, these groups actively avoided their
own feces (“latrine behavior”), but would step on the feces
of zebu and dogs. Ingestion of fecal matter has never been
observed in groups within the reserve, despite over eighteen
years of observations of their feeding ecology (Sauther et
al., 1999). Sifaka were not observed eating any human refuse
and feces, nor have they been observed eating the feces of
domestic animals. Camp ring-tailed lemurs came into close
contact with both humans and their livestock. For example,
they would often feed on the forage brought by humans to
feed zebu (figure 6), thus directly exposing them to zebu
feces. Subsequently contact with livestock occurred with
ring-tailed lemurs but not with sifaka. While sifaka were
usually arboreal, they did come to the ground to cross open
areas in the camp, and to feed on herbs in the reserve.
Parasitology. The preliminary study substantiated
that the lemurs of BMSR harbor parasites (see Table 3). Ectoparasites
were collected from ring-tailed lemurs while they were anesthetized.
These parasites include two species of mesostigmatid mites
(Order Mesostigmata) and one species of tick (Haemaphysalis
lemuris). Fecal examination revealed that this
population of ring-tailed lemurs harbors two species of nematodes,
a pinworm (Oxyuridae, Lemuricola sp.), a species
of strongyles (Lemurostrongylus sp
), and one species of coccida (probably Cryptosporidium;
Graczyk pers.comm.). Physical examinations of anesthetized
ring-tailed lemurs revealed that an unidentified species
of ectoparasite is causing mange on the skin of some individuals.
Mange is a contagious disease that usually results in integument
inflammation and loss of hair (alopecia). At present it appears
that an arthropod parasite (Sarcoptes) is the
source of this mange (Randy Junge, pers. comm.). Of the ring-tailed
lemur samples, 17 of the 70 contained endoparasites. These
were two species of unidentified nematodes, which include
members of the genus Oxyuris and Strongyloides.
All seventy samples of ring-tailed lemurs harbored two unidentified
species of mesostigmatid mites. One species of tick (Haemaphysalis
lemuris), was also common. The Verreaux's sifaka fecal
samples analyzed in 2004 did not contain endoparasites. However
several endoparasites (both nematodes) as well as ectoparasites
have been recovered from work done in 2005. Nevertheless,
endoparasites within the sifaka samples were relatively rare.
No sifaka were anesthetized during the pilot study so no
ectoparasites were obtained, but ticks obtained by Dr. Diane
Brockman and Alison Richard have been identified as Haemaphysalis
lemuris (Brockman, pers.com).
Table 3. Documented parasite species harbored by
the primates at Beza Mahafaly.
by Ring-Tailed Lemurs
by Verreaux's sifaka
Nematode 1 Oxyuridae,Lemuricola sp.
Nematode 1Lemurostrongylus sp.
Scabies** (Sarcoptes sp.)
1Identification by M. Hunter-Ishikawa
2Identification by M. Reichard.
*These are “species specific” parasites. They may have co-speciated
with their host but may use another host accidentally, temporarily,
or as a reservoir.
**Mange was observed on this population
of ring-tailed lemurs but it is unknown if it is due to a
fungal or arthropod parasite (i.e.Sarcoptes). This
is currently being investigated and preliminary results indicate
it is likely to be Sarcoptes mange (Randy Junge,
DVM, pers. comm.).
Human-Nonhuman Primate Interactions. Each
strepsirrhine species interacted with humans differently.
Only one interaction was observed between humans and sifaka.
A male sifaka descended to the ground to cross an open area
camp to get to the forest on the other side of the camp (figure
7). One of the villager's young children was sitting in the
path of the sifaka, who briefly sat down near the child and
looked at him. The child immediately began crying and the
sifaka continued moving toward the forest. The whole interaction
took about 80 seconds. No sifaka were observed using human
food or water. One individual did sit in camp chewing on
a stick of wood (figure 8). In contrast, two groups of ring-tailed
lemurs ranged into the camp and interacted with humans nearly
moving across open area in the camp near parcel 1 of
the Beza Mahafaly Special Reserve.
|Figure 8. Sifaka chewing on wood
within the camp near parcel 1 of the Beza Mahafaly
During this study these “camp” groups drank water
from buckets at the well (figure 9), raided the research
kitchen, ate discarded food at the trash pits or near huts,
and consumed human feces at the open-air latrine. The local
people in camp were usually quite tolerant of the lemurs,
but they would chase them away if the lemurs attempted
to steal food. Ring-tailed lemurs also entered local fields
and ate the leaves of bageda plants on several occasions
during observations. Sifaka were never observed doing this
behavior. We noted 39 human-ring-tailed lemur interactions.
The average interaction was 69 seconds and ranged from
lemurs in the camp near parcel 1 of the Beza Mahafaly
Special Reserve drinking water near the camp's well.
Local Perceptions and Attitudes Toward the Nonhuman
A total of twelve interviews were conducted.
However during each interview local people aggregated and
men and village elders answered questions which were not
directed at themselves. Therefore it is likely that the prestigious
members of the villages influenced the answers of some of
our interviewees. Regardless of these aggregations and our
male-biased interviews, the attitudes, perceptions, origin
myths, and reports of these nonhuman primates' behavior were
almost identical. Among the three villages there existed
small differences regarding how the reserve should be used
In regards to human perception of the primates at Beza
Mahafaly, both species live sympatrically with humans. However
according to our informants, as well as personal observations,
ring-tailed lemurs opportunistically engage in crop raiding
while sifaka do not. Despite these behaviors both the ring-tailed
lemurs and the Verreaux's sifaka enjoy a culturally protected
status. It is this status that may be contributing to the
success of the BMSR. According to our informants, harming,
injuring, eating, or killing these primate species is “fady”
or taboo. The source of these cultural taboos remains unknown,
however our informants provided us with the origin of these
two primate species. According to local folklore, all three
species originated from a single man and his two wives.
man captured a radiated tortoise (Geochelone radiata)
for dinner. He gave the tortoise to his first wife and
left for the day (Figure 10). His second wife became envious
and subsequently, she beat the first wife repeatedly with
a wooden spoon; these beatings ultimately transformed the
first wife into the maky (ring-tailed lemur) (Figures
11 and 12). The first wife, now in the form of a ring-tailed
lemur, grappled with the second wife and beat her with
the wooden spoon until the second transformed into a sifaka
Thus according to our informants' traditional
folklore the ring-tailed lemur and the sifaka were at
one time humans and harming or killing these primates is
forbidden and brings back luck. This protective status is
further reinforced by each species morphological or behavioral
characteristics. The local Mahafaly people have observed
that both species exhibit a reduced rostrum, rely on
vision, and utilize grasping hands that are similar to humans.
Behaviorally our informants said that the maky and
sifaka live in families, fight among each other, and
utter calls to one another. The sums of these characteristics
are not exhibited in other animals according to the people.
Figure 10. Mahafaly origin myth: A man captured a radiated
tortoise (Geochelone radiata) for dinner. He
gave the tortoise to his first wife and left for the
Figure 11. Mahafaly origin myth: His second wife became
envious and subsequently, she beat the first wife repeatedly
with a wooden spoon.
Figure 12. Mahafaly origin myth: these beatings ultimately
transformed the first wife into the maky (ring-tailed
Figure 13. Mahafaly origin myth: The first wife, now
in the form of a ring-tailed lemur, grappled with the
second wife and beat her with the wooden spoon until
the second transformed into a sifaka.
The people that resided at the BMSR interacted with each
species of nonhuman primate differently. These differences
appear to be the result of each species' morphological and
behavioral characteristics. Ring-tailed lemurs exhibit a
wide dietary breadth consuming a broad spectrum of foods
(Sauther et al. 1999). In addition, this species is highly
terrestrial and extremely gregarious. Such characteristics
may result in this species' ability to exist in a wide range
of environments and exploit an expansive range of foods (Sauther
et al. 1999). Based on the feeding ecology, Richard et al.
(1989) assigned members of the genus Macaca into
two distinct categories; “weed” and “non-weed” species. Weed
species benefit from anthropogenic disturbances by utilizing
secondary forests, raiding crops, and exploiting trash pits,
food storages, or kitchens (Richard et al. 1989). Two groups
of ring-tailed lemurs at Beza Mahafaly have utilized human
settlements and while they did feed on some human foods,
unlike some species of “weed macaques,” these groups obtained
the majority of their food from the surrounding forests (Sauther
et al, in press). At best it appears that consuming human
foods, refuse, and human waste (which has never been reported
for ring-tailed lemurs before) allows them to supplement
their diets. In contrast to ring-tailed lemurs, Verreaux's
sifaka are specialized arboreal vertical clinger and leapers
(Richard et al. 1991; 2002). As such they spend much less
time on the ground, where they could directly encounter humans.
However, sifaka who used the camp as part of their home range
did descend to the ground to cross open regions of the camp.
This suggests that behavioral changes in anthropogenically-altered
habitats may increase the potential for parasite infection
in wild strepsirrhines, and is currently being studied. They
were never observed consuming discarded human foods or feces,
raiding trash pits, or drinking at the well. Given there
highly folivorous diet (Richard et al. 1993), it is also
possible that they avoid human foods as this could affect
their microbial fermentation, which is especially important
for folivores (Lambert 1998; Campbell et al. 2002). This
combination of dietary, locomotor, and behavioral traits
resulted in few human-nonhuman primate interactions as compared
to the ring-tailed lemurs.
Both lemur species did exhibit some common behaviors that
may be relevant to parasite prevalence and type. As noted,
both species consumed kily as well as dirt and termite soil.
It has been suggested that consuming these substances combats
endoparasitic infections or ameliorates the pain or discomfort
associated by such infections (Krishnamani and Mahaney 2000;
Carrai et al. 2004; Ketch et al. 2001) or affecting cellulose
digesting gut flora (Norscia et al. 2005). Soil samples are
currently being analyzed for their potential anti-parasitic
properties. Both species were also observed “sunning.” Research
has suggested that sunning effectively eliminates ectoparasites
by raising the ambient temperature beyond the threshold that
the parasite can endure (Blem and Blem 2000). As noted, ring-tailed
lemurs tend to use latrines, i.e. most members defecate and
urinate within the same area. Such behavior could reduce
transmission of fecal parasites among group members and this
is currently being tested.
Each species is also distinctly different in terms of their
behavioral ecology. These differences also influence ethnoprimatological
variables such as human perceptions and attitudes as well
as each species' parasite ecology. For example the wide dietary
breadth of ring-tailed lemurs may allow this species to consume
a broad spectrum of foods, which is beneficial in a harsh,
arid, unpredictable environment when food resources can become
difficult to obtain (Gould et al. 1999; Sauther et al. 1999;
Ratsirarson 2003). As a consequence, incorporating human
refuse and human feces may also provide and maintain a constant
avenue of parasite transmission for species that utilize
oral and fecal-oral routes. Individuals in this population
were diagnosed with two species of nematodes that use oral
routes (Roberts and Janovy Jr. 2000). Given that coprophagy
may be a health concern, the use of feces by ring-tailed
lemurs seems unusual and mal-adaptive. One possibility is
that, because humans and their livestock are relatively new
arrivals to Madagascar, and direct human-lemur interactions
are also relatively recent, negative selection against this
behavior is also recent (Fish, et al. submitted). This requires
more direct analyses but points out the potential for zoonotic
disease transmission to be higher for some lemur species
(Wolfe et al. 1998). The ability to consume a wide spectrum
of foods can also result in primate species engaging in crop
raiding. Human crops are centralized, can cost less to forage,
are low in secondary compounds, and are easy to digest. However
crop-raiding is also a risky behavior that often results
in physical injury or death (Naughton-Treves et al. 1998;
Wheatley et al. 2002). For example, the ring-tailed lemurs
are often chased from crops and are at greater threat from
dog predation when crop-raiding (Sauther, unpublished data).
The Verreaux's sifaka samples contained no endoparasites.
While our sample size for this study is small, two other
studies with much larger samples sizes at this site have
also revealed few to no endoparasites in sifaka (Raveloarisoa
2000 ; Muehlenbein et al. 2003). One possibility is methodological.
Sifaka fecal matter is difficult to process for fecal analyses
and new methods are currently being employed. We know from
our work in 2005 that sifaka do harbor intestinal parasites,
as an adult nematode was recovered (Sauther, unpublished
data). It has also been argued that parasite prevalence may
be low because of their arboreality and lower levels of human-sifaka
interactions (Muehlenbein et al. 2003). These behavioral
characteristics may reduce the likelihood of obtaining environmentally
and socially mediated parasitic infections, and suggests
that this population of sifaka is less prone to parasitic
infections, but this needs to be formally tested across many
seasons. The ring-tailed lemur's samples, in comparison,
exhibited a much higher prevalence of endoparasites overall,
with types that are more likely to be acquired by moving
on the ground or transmitted socially. Ring-tailed lemur
endoparasites such as coccidia are distributed throughout
the hosts' habitat and utilize a fecal-oral (soil) route
to locate a host. Stongyles can be placed in this category
as well, however some species of stongyles will actively
seek a host by honing the temperature gradient of the host
against the outside environment ( Roberts and Janovy 2000
). It is unknown if this species uses the temperature gradient
strategy. Lastly, pinworms require a host to ingest them
or engage in bodily contact. It is also possible that the
higher parasite prevalence and increased parasite diversity
exhibited by these ring-tailed lemurs are related to differences
in ecology. As ring-tailed lemurs at BMSR utilize a wider
range of habitats, including areas that bring them into higher
contact with domestic animals (Fish, et al. submitted), they
are thus potentially exposed to a wider range of parasites.
This is being currently investigated.
It is important to note that results from paleontological
research in the area indicate that local people have not
always viewed lemurs asfady. Evidence of butchery
from a nearby area, Taolambiby, exists for subfossil forms
(Paleopropithecus and Pachylemur) and
extant Propithecus. There is no evidence of butchery
of ring-tailed lemurs, however, which is uncommon in the
Taolambiby assemblage (Perez et al. 2005). These fossils
from Taolambiby date to a little over 2000 years ago (Burney
et al. 2004). Today both the sifaka and ring-tailed lemur
figure prominently in the local Mahafaly origin myths and
are protected by cultural beliefs offady. Several
young villagers were unaware that the lemurs are endemic
to Madagascar and occur nowhere else in the world. Once informed
of this endemism, some villagers took pride in the uniqueness
of these species. Our informants generally felt positive
toward the reserve and claimed the forest at Parcel 1 is
sacred and houses sacred animals. In addition, the reserve
provides jobs for members of the neighboring villages and
in times of emergency the reserve's car can be utilized.
Although the results of our interviews suggested that the
reserve is protected and these primates enjoy a protected
status we observed traces of grazing (zebu tracks and feces)
at the edges of the reserve and on rare occasions small trees
are cut down. Local people may not associate the link between
habitat destruction and its detrimental effects on viability
of this population, and/or the traditions and origins they
provided lie in the realm of the “ideal” and are not always
practiced. In addition elders of Manasoa feel it is their
right to graze their livestock in the reserve, as the land
once belonged to this village. Nevertheless, most of the
reserve remains intact with little human induced change.
While such cultural traditions currently provide these
primates at Beza Mahafaly with a protective status, which
is beneficial for long-term conservation initiatives, not
all Malagasy groups share this perspective. The relationship
between lemurs and the Malagasy vary across the island. In
some areas formal dina or rules against hunting
exists (Henkels 2002) but poaching is on the rise (Pettus
2005). For example, the results of our ethnographic fieldwork
are in stark contrast to the findings by Simons and Meyers
(2001) who investigated local peoples' perceptions of the
aye-aye (Daubentonia madagascariensis) at villages
d'Ambre in northern Madagascar. According to local peoples
in this region the aye-aye isfady and if an aye-aye
enters a village it may cause sickness or death (Simons and
Meyers 2001). In some villages if an aye-aye is seen, it
must be killed and its body or tail must be hung from a pole
at a crossroad to avoid bad luck to the village (Simons and
Meyers 2001; Koenig 2005). Among villages there is variation
regarding how to remedy the bad luck associated with the
aye-aye, however each village believed that the aye-aye is
evil. These beliefs have obvious detrimental effects on the
small remaining populations of aye-ayes in Madagascar. It
also points out the far-reaching effects of cultural perceptions
on the survival of lemurs in Madagascar. Unfortunately, protective
cultural practices such as the fady against harming
lemurs at Beza Mahafaly may be tenuous. In many areas of
Madagascar where such fady have protected lemurs,
these cultural traditions may be breaking down due to poverty
and diet (Pettus 2005).
We thank de La Prairie, Enafa Efitroaromy, Ehandidy Ellis, Razanajafy
Olivier, Emady Rigobert, and Elahavelo of the Beza Mahafaly
Ecological Monitoring Team, Frank Cuozzo, Mandala Hunter-Ishikawa,
and Kerry Sondgeroth, for their assistance with data collection
at Beza Mahafaly during the 2004 field season. We thank Dave
Miller, Robert W. Sussman, Joel Ratsirarson, Jo Ajimy, Randrianarisoa
Jeannicq, Dr. Rafidisoa Tsiory (ANGAP), and Thaddeus Graczyk
for their strong support and facilitation of our project.
Our appreciation also goes to the Département des
Eaux et Forêts, Ecole Superieur des Sciences Agronomiques,
Université d'Antananarivo and ANGAP for allowing us
to continue our research at Beza Mahafaly. We than Dennis
McGilvray and three anonymous reviewers who provided very
thoughtful and valuable comments. Funding for this study
came from the Lindbergh Fund, The Saint Louis Zoo, The John
Ball Zoo Society, The National Geographic Society, and the
University of Colorado, Boulder (Department of Anthropology
and the William H. Burt Fund).
Altmann, J. 1974. Observational study of behaviour: sampling
methods. Behaviour 49:227-267.
Alvard, M.S., J.G. Robinson, K.H. Redford, and H. Kaplan.1997.
The sustainability of subsistences hunting in the Neotropics.
Conservation Biology 11: 977-982.
Ash, L.R., and T.C. Oriel. 1987. Parasites: a guide to laboratory
procedures and identification. Chicago: American Society
of Clinical Parasitologists Press.
Benard, H.R. 2000. Research Methods in Anthropology: Qualitative
and Quantitative Approaches. Thousand Oaks: Sage Publications.
Burney DA, Burney LP, Godfrey LR, Jungers WL, Goodman SM,
Wright HT, Jull AJT. 2004. A chronology for late prehistoric
Madagascar. J Hum Evol 47:25-63.
Burton, F.D. 2002. “Monkey King in China: basis for conservation
policy?” In Primates Face to Face: The Conservation Implications
of Human-Nonhuman Primates Interconnections. Edited by A.
Fuentes and L.D. Wolfe, pp. 137-162. Cambridge: Cambridge
Campbell, J. L., Williams, C. V. and Eisemann J. H. 2002.
Fecal inoculum can be used to determine the rate and extent
of In Vitro fermentation of dietary fiber sources across
three lemur species that differ in dietary profile:Vareciavariegata,Eulemur
fulvus andHapalemur. Journal of Nutrition.
Carter, A., and C. Carter. 1999. “Cultural representations
of nonhuman primates,” In The Nonhuman Primates. Edited by
P. Dolhinow and A. Fuentes, pp. 270-276. Mountain View: Mayfield
Chapman, C.A., S.R. Balcomb, T.R. Gillespie, and J.P. Skorupa.
2000. Long-term effects of logging on African primate communities:
a 28-year comparison from Kibale National Park, Uganda. Conservation
Cormier, L.A. 2002. “Monkey as food, monkey as child: Guaja
symbolic canabalism,” In Primates Face to Face: The Conservation
Implications of Human-Nonhuman Primates Interconnections.
Edited by A. Fuentes and L.D. Wolfe, pp. 63-84. Cambridge:
Cambridge University Press.
Durante-Quiroga, A., and A. Estrada. 2003. Primates as pets
in Mexico City: an assessment of the species involved, source
of origin, and general aspects of treatment. American Journal
of Primatology 61:53-60.
Ganzhorn J.U., P.C. Wright, and J. Ratgsimbazafy. 1999.
“Primate communities: Madagascar,” In Primate Comunities.
Edited by J.G. Fleagle, C. Janson, and K. Reed, pp. 75-89.
Cambridge: Cambridge University Press.
Gould, L., R.W. Sussman, and M.L. Sauther. 1999. Natural
disasters and primate populations. The effects of a two-year
drought on a naturally occurring population of ring-tailed
lemurs (Lemur catta) in Southwestern Madagascar.
International Journal of Primatology 20: 69-84.
Henkels, D. 2002. A Close Up of Malagasy Environmental Law.
Vermont Journal of Environmental Law, Volume Three. (On-line
Irwin MT, Samonds KE, Raharison J, Wright PC. 2004. Lemur
latrines: observations of
latrine behavior in wild primates and possible ecological
significance. Journal of Mammalogy 85:420-427.
Fish, K, Sauther M.L. and Joudon, J. Allocoprophagy in wild
ring-tailed lemurs (Lemur catta) in human-disturbed
locations adjacent to the Beza Mahafaly Special Reserve,
Madagascar. Submitted to American Journal of Primatology.
Fleagle, J.G. 1999. Primate Adaptation and Evolution. San
Diego: Academic Press.
Fuentes A., L.D. Wolfe. 2002. “Cultural views of nonhuman
primates,” In Primates Face to Face: The Conservation Implications
of Human-Nonhuman Primates Interconnections. Edited by A.
Fuentes and L.D. Wolfe, pp. 61-62. Cambridge: Cambridge University
Jolly, A. 2003. “Lemur catta, Ring-tailed lemur,Maky,”
in The Natural History of Madagascar. Edited by S.M. Goodman
and J.P. Benstead, pp. 1329-1331. Chicago: University of
Jones-Engel, L., G.A. Engel, M.A. Schillaci, R. Babo, and
J. Froehlich J. 2001. Detection of antibodies to selected
human pathogens among wild and pet macaques (Macaca
tonkeana) in Sulawesi, Indonesia. American Journal
of Primatology 54: 171-178.
Jones-Engel, L., M. Schillaci, and G. Engel. 2003. “Human-nonhuman
primate interactions: an ethnoprimatological approach,” In
Field and Laboratory Methods in Primatology: A Practical
Guide. Edited by J.M. Setchell and D.J. Curtis, pp. 15-24.
Cambridge: Cambridge University Press.
Karanth, K.P., Delefosse T. Rakotosamimanana B., Parsons
T.J. & Yoder A.D. 2005.
Ancient DNA from giant extinct lemurs confirms single origin
of Malagasy primates
Proceedings of the National Academy of Sciences 102: 5090–5095.
Koenig P. 2005. Découverte d'une dépouille
de Aye-aye (Daubentonia madagascariensis) dans
le nord-ouest de Madagascar. Lemur News 10: 6-7.
Lambert, J.E. 1998. Primate Digestion: Interactions Among
Physiology, and Feeding Ecology. Evolutionary Anthropology
Loudon, J.E., M.E. Howells, A. Fuentes. In press. The importance
of integrative anthropology: a preliminary investigation
employing primatological and cultural anthropological data
collection methods in accessing human-monkey co-existence
in Bali, Indonesia. Ecological and Environmental Anthropology.
Muehlenbein, M.P., M. Schwartz, and A. Richard. 2003. Parasitologic
analyses of the sifaka (Propithecus verreauxi verreauxi)
at Beza Mahafaly, Madagascar. Journal of Zoo and Wildlife
Naughton-Treves, L., A. Treves, C. Chapman, and R. Wrangham.
1998. Temporal patterns of crop raiding by primates: linking
food availability in croplands and adjacent forest. Journal
of Applied Ecology 35:596-606.
Norscia, I., Carrai, V., Ceccanti, B., Borgognini Tarli,
S.M., 2005. Termite soil eating in Kirindy Sifakas (Madagascar):
Proposing a new proximate factor. Folia Primatologica 76:119-122.
Perez VR, Godfrey LR, Nowak-Kemp M, Burney DA, Ratsimbazafy
J. Vasey N. 2005. Evidence of early butchery of giant lemurs
in Madagascar. J Hum Evol 49:722-742.
Pettus, A. 2005. Wild Harvest: A Taste for Extinction. Harvard
Magazine 107 (6) (on line publication: http://www.harvardmagazine.com/on-line).
Rambeloson FR 1988. Contribution à l ´ etude
de l´utilisation des ressources forestieres aux environs
de la Reserve Special de Beza Mahafaly (Cas du village Analafaly)
Mémoire de fin d´etudes, Establilssement d´Enseignement
Supérieur des Sciences Agronomiques, Université d´Antananarivo.
Raveloarisoa, A. 2000 . Contribution à l´etude
de la préférence alimentaire duPropithecus
verreauxi verreauxide la Réserve Spéciale
de Beza Mahafaly (Parcelle I). Mémoire DEA. Département
de Biologie Animale (Option Ecologie Animale-Environnement),
Faculté des Sciences. Univ. d ´ Antananarivo,
Ratsirarson, J. 2003. “Réserve Spéciale de
Beza Mahafaly,” In The Natural History of Madagascar. Edited
by S.M. Goodman and J.P. Benstead, pp. 1520-1525. Chicago:
University of Chicago Press.
Richard, A.F., S.J. Goldstein, and R.E. Dewar. 1989. Weed
macaques: the evolutionary implications or macaque feeding
ecology. International Journal of Primatology 10: 569-594.
Richard, A.F., P. Rakotomanga, and M. Schwartz. 1991. Demography
ofPropithecus verreauxiat Beza Mahafaly Madagascar:
sex ratio, survival, and fertility 1984-1988. American Journal
of Physical Anthropology 84: 307-322.
Richard, A.F., P. Rakotomanga, and M Schwartz. 1993. Dispersal
byPropithecus verreauxiat Beza Mahafaly Madagascar”
1984-1991. American Journal of Primatology 30: 1-20.
Richard, A.F., R.E. Dewar, M. Schwartz, and J. Ratsirarson.
2002. Life in the slow lane? Demography and life histories
of male and female sifaka (Propithecus verreauxi).
Journal of the Zoological Society of London256:
Roberts, L.S., and J. Janovy Jr. 2000. Foundations of parasitology.
Boston: McGraw-Hill Press.
Sauther, M.L. 1991 Reproductive behavior of free-rangingLemur
cattaat Beza Mahafaly Special Reserve, Madagascar.
American Journal of Physical Anthropology 84: 463-477.
Sauther, M.L. 1993. “Changes in the used of wild plants
foods in free-ranging ringtailed lemurs during lactation
and pregnancy: some implications for early hominid foraging
strategies,” In Eating on the Wild Side: The Pharmacologic,
Ecologic, and Social Implications of Using Noncultigens.
Edited by N.L. Etkin, pp. 240-256. Tucson: University of
Sauther, M.L. 1999. “The interplay of phenology and reproduction
in ringtailed lemurs: implications for ringtailed lemur conservation,”
In Biology and Conservation of Prosimians, Folio Primatologica
69 (Supplement 1). Edited by C.S. Harcourt, R.H. Crompton,
and A.T.C. Feistner ATC, pp. 309-320.
Sauther, M.L., R.W. Sussman, and L. Gould. 1999. The socioecology
of the ringtailed lemur: thirty-five years of study. Evolutionary
Sauther, M. L., K. D. Fish, F. P. Cuozzo, D. S. Miller,
M. Hunter-Ishikawa, and H. Culbertson. In press. Patterns
of health, disease, and behavior among wild ring-tailed lemurs,Lemur
catta: effects of habitat and sex. In:Jolly A, Koyama
N, Rasamimanana H, and Sussman RW. (eds.). Ring-tailed Lemur
Biology. Springer, New York, New York.
Sicotte, P., and P. Uwengeli. 2002. “Reflections on the
concept of nature and gorillas in Rwanda: implications for
conservation,” In Primates Face to Face: The Conservation
Implications of Human-Nonhuman Primates Interconnections.
Edited by A. Fuentes and L.D. Wolfe, pp. 163-182. Cambridge:
Cambridge University Press.
Simons, E., and D. Meyers. 2001. Folklore and beliefs about
the aye-aye (Daubentonia madagascariensis). Lemur
Sponsel, L.E. 1997. “The human niche in Amazonia: explorations
in ethnoprimatology,” In New World Primates: Ecology, Evolution,
and Behavior. Edited by W.G. Kinzey, pp. 143-165. New York:
Aldine de Gruyter.
Sponsel, L.E., N. Ruttanadakul, and P. Nadadecha-Sponsel.
2002. “Monkey business? The conservation implications of
macaque ethnoprimatology in Southern Thailand,” In Primates
Face to Face: The Conservation Implications of Human-Nonhuman
Primates Interconnections. Edited by A. Fuentes and L.D.
Wolfe, pp. 288-309. Cambridge: Cambridge University Press.
Sussman, R.W. 1991. Demography and social organization of
free-rangingLemur catta in the Beza Mahafaly Reserve,
Madagascar. American Journal of Physical Anthropology 84:
Sussman, R.W. 1999. Primate Ecology and Social Structure:
Volume 1: Lorises, Lemurs and Tarsiers. Massachusetts: Pearson
Tattersall I. 1982. The Primates of Madagascar. New York:
Columbia University Press
Wheatley, B.P. 1999. The Sacred Monkeys of Bali. Illinois:
Wheatley, B.P., R. Stephenson, H. Kurashina, and K. Marsh-Kautz.
2002. “A cultural primatological study ofMacaca fascicularis on
Ngeaur Island, Republic of Palau,” In Primates Face to Face:
The Conservation Implications of Human-Nonhuman Primates
Interconnections. Edited by A. Fuentes and L.D. Wolfe, pp.
240-253. Cambridge: Cambridge University Press.
Whitelaw DC, Sauther ML, Loudon JE, Cuozzo F. 2005. Anthropogenic
change in and around Beza Mahafaly Reserve: methodology and
results. American Journal of Physical Anthropology. Supplement
Wolfe, N.D., A.A. Escalante, W.B. Karesh, A. Kilbourn, and
A. Lal. 1998. Wild primate populations in emerging infectious
disease research: the missing link? Emerging Infectious Diseases
Workman, C. 2004. Primate conservation in Vietnam: toward
a holistic environmental narrative. American Anthropologist
By 2005 ANGAP had reduced village occupation. Today there
is only one family on site and no poultry.