Feeding outside the forest- Importance of crop raiding and an invasive species in the
diet of gallery forest Lemur catta following a cyclone at the Beza Mahafaly Special
Reserve, Madagascar.
LaFleur, Marni. University of Victoria (M.Sc. candidate).
ABSRACT
While examining feeding and nutrition of male and pregnant female L. catta, I
collected data on crop raiding and foraging on the invasive weed, Argemone mexicana L.
In January of 2005, a cyclone swept through southern Madagascar and the Beza
Mahafaly Special Reserve. Cyclone activity at Beza coincided with flowering of
Tamarindus indica L., which consequently almost completely failed to fruit; leaving L.
catta without their major food resource during the both dry and reproductive season. I
followed two adjacent groups (Red and Green) and observed that both ventured outside
of the forest reserve to secure food. The home range of Red group (RG) included a
farmer’s crop, from which the animals fed daily on both A. mexicana and
Convolvulaceae sp. leaves (an agricultural product). The home range of neighboring
Green group (GG) did not include the crop; however they did feed daily on A. mexicana,
which also grew in the dry river bed (outside of the forest). GG spent significantly more
time foraging (p=0.004), although there was no significant difference between overall
estimates of amount eaten for the groups. When compared to GG, RG spent significantly
more time feeding in the crop (p=0.004) and ingested more in the crop (p=0.003). There
was no difference between RG and GG time spent feeding in the forest, although GG
ingested significantly more in the forest (0.015). As such, it appears that although A.
mexicana was an important food for both groups, Convolvulaceae was an especially
important resource for RG. Implications include insight into the plasticity of primates
when foraging in an ever changing environment, benefits of crop raiding, and on the use
and proliferation of an invasive floral species.
INTRODUCTION
In order to access if the nutritional intake of male and female L. catta reflected
that of their feeding behavior (as outlined by Sauther 1994, 1998), I collected data on
feeding behavior and also collected plant samples for nutritional analyses. However, this
study occurred in a non-typical season, because in late January of 2005 the tropical
cyclone Ernest swept over Madagascar’s south, resulting in sustained winds of 100 km/hr
(60 m/h) and severe flooding which originated in the Southwestern city of Tulear
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(Stevens, 2005). At the Beza Mahafaly Special Reserve, staff recorded flood waters of
over a meter, and noted winds resulted in significant tree and plant damage and
defoliation (Razanajafy and Raznadrainy, pers comm). Notably, the storm coincided with
peak flowering of T. indica at Beza (Razanajafy and Raznadrainy, pers comm), which
subsequently almost completely failed to fruit (LaFleur, pers obsv).
Madagascar is characterized by its harsh and unpredictable environment in which
cyclones, storms, drought, and other natural disasters plague the island (Ganzhorn et al.,
1999). Lemurs have evolved a suite of traits, such as reproductive synchrony, and female
dominance and feeding priority, which allow them to best cope with environmental and
resource uncertainty (Jolly, 1984; Wright, 1999). Ring tailed lemurs are opportunistic
frugivore/folivores that exploit a variety of plant and non-plant based resources, at all
levels of the forest, as those resources become annually available (Sauther, 1994, 1999).
Despite being flexible foragers, ring tailed lemurs are highly dependant on either young
leaves or fruits from T. indica, which are produced asynchronously and are present
throughout the year (Sauther, 1998).
Tamarindus indica fruits and young leaves are both a rich source of protein;
however, T. indica fruits are of utmost importance in L. catta diet in August through
October as a) T. indica young leaves are not available, b) this is the height of the dry
season, and c) late gestation period for females (Sauther, 1993). Female ring tailed lemurs
are thus at negative energy balance, through the combination of dry season related
reduction in food availability, and the increased metabolic requirements of gestation
(Sauther, 1993). How then does L. catta meet metabolic requirements in times without T.
indica fruits or young leaves? This paper examines the response of two groups of male
2
and late-term pregnant L. catta females to a post-cyclone dry season, in which T. indica
fruits are nearly absent.
METHODS
The Beza Mahafaly Special Reserve is located in southwestern Madagascar, and
consists of a primary 1km2 parcel of forest bordering the Sakamena river (Fig. 1). The
reserve was established in 1978 and deemed a Special Government Reserve in 1985
(Sussman, 1991). The climate is highly variant with a cool/dry season (June to August), a
hot/wet season (November to March), and transitional periods in between (Sauther, 1992;
Sussman, 1991). The eastern portion of the reserve contains xerophytic (spiny) forest
which is dominated by Euphorbia tirucalli, while the western portion of the reserve is
gallery forest where T. indica dominates the landscape (Sauther, 1998). Both forest types
host a plethora of tree species, vines and herbaceous plants. In the dry season, the
Sakamena river bed is waterless and becomes quickly populated with the fast growing,
drought resistant and invasive weed A. mexicana.
3
Figure 1. Trail map and
location of the Beza
Mahafaly Special
Reserve, Madagascar.
Over a one month period from August 9 to September 7, 2005, I collected data on
all adult animals of two distinct neighboring social groups residing in the gallery forest.
Both group’s home ranges bordered the Sakamena River, and the RG’s home range also
included a farmer’s crop (Fig. 2). I recorded 10 focal sessions (Altmann, 1974) of 15
minute intervals per animal, and to ensure equal distribution of sampling, individual
animals were rotated and groups were alternated each day. When a focal animal was
feeding, I noted the animal’s location, amount eaten (number of leaves or bites), and the
plant and plant part ingested, and subsequently collected representative food samples
4
(except for T. indica fruits, which were too limited to collect). I deemed a group to be
foraging when 80% or more of its members were actively manipulating or eating foods.
Before collecting data and plant samples in the farmer’s crop, I gained permission and
subsequently asked how the farmer felt about lemur crop raiding.
Figure 2. Pictorial of
Red and Green Groups’
home ranges, along
with locations of crop,
dry river bed and forest.
All plants collected were dried in the shade and identified by a local Malagasy
botanist (Elahavelo), and were later analyzed for their nutritional content at the Dairy
One Forage Laboratory1. For the purposes of this paper only the nutritional content of
Convolvulaceae and A. mexicana will be considered. In order to estimate the mass of a
plant part eaten, I weighed 10 dried plant samples to find the part average and then
multiplied the number of leaves or bites an animal took by the average plant part mass.
Elahavelo collected phenological data of the RG and GGs’ gallery forest habitat,
once at the onset of and again at the end of my study period. Using line transects, he
5
identified 140 large (greater than 20cm in diameter at breast height) trees (excluding T.
indica), by species or local name, and scored trees for presence of flowers and fruit.
Additionally, Elahavelo surveyed 105 T. indica trees within for presence or absence of
fruit and scored the ripeness of fruits. Since T. indica was not flowering and there was a
lack of young leaves in all trees, these variables were not surveyed.
I used the Mann-Whitney U test to compare probability distributions of RG and
GGs’ overall time spent foraging and amounts eaten, and to compare the two groups’
time spent foraging and grams eaten by location (forest or crop). Since the RG did not
forage in the river bed, no comparisons between groups were made in this habitat.
RESULTS
The farmer (name unknown) whose crop RG raided daily, said that he did not
want the lemurs in his field, and that before the Reserve was protected he and other
farmers would have tried to kill a lemur that was eating crop foods. However, now that
the lemurs are protected, he would either do nothing when they were eating in the crop or
maybe through a rock at them, with only the intention of scaring them away.
Argemone mexicana had higher percentages of crude protein, total digestible
nutrients2 and all minerals except Calcium when compared to Convolvulaceae (Table 1).
However, the leaves of A. mexicana were armed with sharp thorns and spines, which
decreased foraging efficiency through increased processing time.
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Table 1. Percents of Crude Protein, Total Digestible Nutrients, Calcium, Phosphorus, Magnesium,
Potassium, and Sodium present in A. mexicana and Convolvulaceae.
% Crude
% Total Digestible
% Ca % P % Mg % K
% Na
Protein
Nutrients
A. mexicana
29.5
65
1.45
.34
.38
4.03
.021
Convolvulaceae
20.8
62
1.73
.19
.34
2.44
.009
Of the 140 sampled trees (excluding T. indica), 62 had flowers present (48
initially and 62 at the end of the study period), but none had fruits, and as mentioned,
there were few young leaves. Of the 105 T. indica trees samples only 2 had fruits
(ripeness 2 on a scale of 1-5, where 1=complete unripe and 5=ripe). The crop consisted of
approximately 20% A. mexicana, and 80% Convolvulaceae plants, which the RG
aggressively defended against GG and other neighboring groups’ repeated attempts at
access.
RG spent 37% of their focal time feeding, while GG spent 54% of their focal time
feeding, which was significantly more (Mann Whitney U= 8, n1=11, n2=7, p=0.004).
Estimates of overall amount eaten show no significant difference between groups. RG did
not forage in the dry river bed; rather they spent 47% of their foraging time in the
farmer’s crop and 53% in the forest. GG spent 6% of their foraging time in the crop
(which they accessed when the RG was not present), 17% of their foraging time in the
dry riverbed, and 78% in the forest. There was no significant difference between the time
spent feeding by the RG and GG in the forest habitat, but RG spent significantly more
time than the GG feeding in the crop (Mann Whitney U=8, p=0.004). GG ate
significantly more in the forest than the RG (Mann Whitney U=19, p=0.015), while RG
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ate significantly more in the crop than the GG (Mann Whitney U=7, p=0.003). Both
groups spent small amounts of their feeding time eating T. indica (RG=2%, GG=1.6%).
DISCUSSION
Phenotypic plasticity is a potential mode for a taxon to colonize a broad
ecological niche (Ménard, 2002). The ability to exploit a wide variety of resources may
be an evolutionary trait which is favored in unpredictable environments, such as
Madagascar (Wright, 1999). The extreme limits of L. catta ecological plasticity may
present in the high mountain populations of the Andringitra Massif region where plant
distribution is described as low ericoid bush and sub-alpine (Goodman and Langrand,
1996), making it quite different from plant distribution in all other L. catta locations.
Dietary plasticity, as found L. catta, may be a key feature enabling the species to persist
in environmental change.
Lemur catta reproduction is highly tied to seasonal resources (Rasamimanana and
Rafidinarivo, 1993; Sauther, 1992, 1993, 1998; Yamashita, 2002). Females are in late
gestation during the driest parts of the year (Sauther, 1994, 1998) and normally depend
on the keystone resource T. indica as it is a reliable source of protein and other essential
nutrients (Sauther, 1992; Mertl-Millhollen et al., 2003). However, T. indica fruits were
almost completely absent and young leaves were not available during the present study.
Introduced and cultivated plants appear to play an important role in L. catta diet,
in the absence of T. indica fruits. Similarly, Soma (1994) found that introduced species at
Berenty Reserve reduced the effect of extreme food seasonality in gallery forest.
Comparative ease of processing is most likely why RG combatively guarded the
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Convolvulaceae sp. crop plants, instead of concentrating foraging on A. mexicana, which
is more abundant and higher in both crude protein and most measured minerals.
Furthermore, extensive processing time required when foraging on A. mexicana is most
likely why GG spent more time foraging, even though they did not eat more than RG.
Argemone mexicana seeds are highly toxic (Pahwa and Chatterjee, 1989) and were not
eaten by L. catta, but the seeds often spilled during leaf processing, which subsequently
got caught in the lemurs’ fur (LaFleur, pers obsv). Albeit a widely distributed and
successful invasive species, the local proliferation of A. mexicana at Beza is likely aided
through lemur seed dispersal.
Risks of foraging outside the forest include threat from humans (Saj et al., 2001),
increased predation pressure (Sauther, 2002), and in the case of feeding in the crop, risk
of injury defending the highly coveted territory. Since female lemurs are responsible for
the majority of combative territory defense (Jolly et al., 1993; Koyama, 1991; MertlMillhollen et al., 1979; Nakamichi and Koyama, 1997), they have more at stake when
protecting home ranges, especially if they are pregnant or if they have an infant (MertlMillhollen et al., 2003). However, the cost of defending the crop territory in the case of
RG may have been offset by the frequent presence of humans in the area. Since farmers
are generally not aiming to injure crop raiding lemurs, but may keep aerial predators at
bay, predation pressure that is generally elevated out of the forest, may be reduced when
in the crop.
Ecological plasticity as an adoption to living in an unstable environment may
enable L. catta to exploit new and non-native foods during times of food scarcity and
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following natural disasters. Follow-up censuses of L. catta at the Beza Mahafaly Special
Reserve will determine the full effects of a reproductive season without T. indica.
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Footnotes
1. Complete methods from the Dairy One Forage Laboratory available at
http://www.dairyone.com/Forage/Procedures/default.htm
2. Total digestible nutrients denotes the sum of the digestible protein, digestible
nitrogen-free extract, digestible crude fiber and 2.25X the digestible fat (National
Research Council, 1988).
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