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Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 124:234 –247 (2004)
Diet and Nutrition in Wild Mongoose Lemurs (Eulemur
mongoz) and Their Implications for the Evolution of
Female Dominance and Small Group Size in Lemurs
Deborah J. Curtis*
School of Life Sciences, University of Surrey Roehampton, London SW15 3SN, UK
KEY WORDS
Madagascar
feeding behavior; phytochemistry; seasonality; nutritional stress; frugivory;
ABSTRACT
Data collected on the feeding behavior,
food intake, and chemical analyses of plant foods were
used to document seasonal variation in diet and nutrition
in Eulemur mongoz in northwestern Madagascar. E. mongoz conforms to the general Eulemur dietary pattern, with
a predominantly frugivorous diet supplemented mainly by
leaves, flowers, and nectar. Phytochemical analysis revealed high water contents in all the main plant foods;
mature fruit and flowers contained the most water-soluble
carbohydrates; immature leaves were richest in protein
and essential amino acids; the limiting amino acids in all
plant foods were methionine and cystine; ash (mineral)
content was highest in petioles and mature leaves; crude
lipid content was highest in seeds; and crude fiber content
was indistinguishable between immature and mature
fruit and leaves. High-fiber foods were eaten during both
Seasonal variability in the availability of important food resources has been linked to the life history of lemurs and has been used to explain the
evolution of unusual aspects of lemur behavior, such
as female dominance and small group size. In this
paper, I investigate seasonal differences in feeding
behavior in the mongoose lemur (Eulemur mongoz)
through a comparison of time spent feeding, food
items eaten, and food intake during the wet and dry
seasons. Furthermore, I assess phytochemical differences among plant parts consumed, and based on
the chemical analysis of these food items, I quantify
nutrient intake and use these data to investigate
seasonal variation at the chemical level.
Reproduction in all but a few species of lemurs
(Sterling, 1994; Curtis et al., 2000) is strictly seasonal; the onset of the breeding season is photoperiodically induced and lasts 1–2 months (Van Horn,
1980; Lindberg, 1987). Gestation and in some cases
lactation occur during periods of assumed food scarcity. It was therefore suggested that lemur females
may suffer from, or have evolved tactics for avoiding
seasonally induced nutritional stress imposed by a
lack of resources. This forms the basis for the “energy conservation hypothesis,” proposed to explain
the prevalence of female dominance and small group
©
2004 WILEY-LISS, INC.
seasons; the wet season diet was dominated by high-energy foods (mature fruit, nectar, and seeds), while the dry
season diet contained foods high in energy (mature fruit
and flowers) and high in protein (immature leaves) and
minerals (mature leaves and petioles). However, nutrient
intake did not vary between seasons, implying that nutrient requirements are met throughout the year. These
results suggest we draw more conservative conclusions
when interpreting dietary variability in the absence of
chemical analysis, and also draw into question the idea
that nutritional stress is a factor in the timing of reproduction in lemurs and, by extension, is linked to the prevalence of female dominance and small group size in lemurs. Am J Phys Anthropol 124:234 –247, 2004.
©
2004 Wiley-Liss, Inc.
size in lemurs. Adult females dominate males in
most lemur species and have priority of access to
food, which may have allowed females to cope with
high reproductive costs when energy supplies are
low (Jolly, 1984; Richard and Nicoll, 1987; Young et
al., 1990; Meyers and Wright, 1993; Pereira et al.,
1999). Group size in lemurs, as in other primates,
may be correlated with the distribution of food resources (Terborgh, 1983; Overdorff, 1996), and small
group size could be a result of constraints imposed
by a nutritionally stressful environment (Wright,
Grant sponsor: A.H. Schultz-Stiftung; Grant sponsor: G. & A.
Claraz-Schenkung; Grant sponsor: Goethe Stiftung; Grant sponsor:
Schweizerische Akademie der Naturwissenschaften; Grant sponsor:
Primate Conservation, Inc.; Grant sponsor: Bundesamt für Bildung
und Wissenschaft, Bern, Switzerland; Grant number: AIR3-CT942107.
*Correspondence to: Deborah J. Curtis, School of Life Sciences,
University of Surrey Roehampton, West Hill, London SW15 3SN, UK.
E-mail: d.curtis@roehampton.ac.uk
Received 18 July 2001; accepted 3 January 2003.
DOI 10.1002/ajpa.10268
Published online 3 November 2003 in Wiley InterScience (www.
interscience.wiley.com).
DIET AND NUTRITION IN EULEMUR MONGOZ
1986). An increase in lemur group size is accompanied by an increase in intragroup competition over
access to food (e.g., Wright, 1999), which would be
disadvantageous to females when food availability is
low.
Wright (1999) more recently proposed extending
the “energy conservation hypothesis” and reconsidering it as an “energy frugality hypothesis.” Wright
(1999) postulated that female dominance, small
group size, and other lemur traits may also represent adaptations to maximize the use of scarce resources. For example, the synchronization of weaning with food abundance appears to be a priority in
lemur life histories (Wright, 1999). Pereira et al.
(1999) dispute the fact that female lemurs might
experience any more or less stress during reproduction than other comparable mammals. In fact, as
pointed out by Pereira et al. (1999), the term “stress”
is misplaced, as this is based on the assumption that
animals exploit food resources in order to fulfill only
maintenance functions, such that when confronted
with food scarcity, nutrient demands cannot be met
(King and Murphy, 1985). If, as suggested by Wright
(1999), food resources are maximally exploited during periods of abundance, then sufficient reserves
will be built up to tide over periods when less nutritious foods are available (King and Murphy, 1985),
and behavioral, anatomical, and physiological mechanisms will aid in the conservation of energy
(Pereira et al., 1999).
Lemurs in the genus Eulemur (family: Lemuridae) either live in small multimale, multifemale
groups or are socially monogamous. Eulemur sp. are
predominantly frugivorous throughout all types of
habitat in Madagascar, and therefore the discussion
of seasonal dietary adjustments has often focused on
periods of fruit scarcity and/or the dry season, which
usually overlap with the energetically costly reproductive phases of gestation and/or lactation. However, Eulemur sp. exhibit habitat-dependent differences in the extent of frugivory and in how this diet
is complemented in different seasons by leaves, flowers, and nectar between the rainforests of eastern
Madagascar (Overdorff, 1993; Vasey, 2002), the
rainforests of the Northwest (Freed, 1996; Andrews
and Birkinshaw, 1998), and the seasonally dry forests of the West and the Comorian island Mayotte
(Sussman, 1974; Tattersall, 1977; Andriatsarafara,
1988; Colquhoun, 1997; Donati et al., 1999; Rasmussen, 1999). Given the variability in dietary strategies pursued by these closely related lemurs in different habitats, it is difficult to use this information
on food-item consumption alone for the investigation
of what effect seasonality may have had on the evolution of lemur traits such as female dominance and
small group size. If we assume an animal will ensure
that its nutrient requirements are always met and
that seasonally induced nutritional stress is indeed
fiction rather than fact (King and Murphy, 1985),
then this seasonal variability in food items con-
235
sumed may not be mirrored by seasonal variability
in nutrient composition and food intake.
Current knowledge of nutrient composition in lemur diets in the wild is limited to Hapalemur griseus alaotrensis (Mutschler, 1999), Daubentonia
madagascariensis (Sterling et al., 1994), Lemur
catta and Propithecus verreauxi verreauxi (Yamashita, 2002), and a comparative study of seven
species of lemur in an eastern Malagasy rainforest
(Ganzhorn, 1988). Fruit and nectar are generally
regarded as the main source of carbohydrates and
lipids, while leaves, flowers, and seeds provide protein, minerals, and vitamins, with protein intake
potentially boosted by consumption of animal matter (Waterman, 1984). Periods of fruit scarcity in
Eulemur diets would therefore be translated into a
scarcity of high-energy carbohydrates and lipids
during energetically costly reproductive phases.
However, Pereira et al. (1999) suggested that perhaps flowers and new leaves might be crucial to
female reproductive success. Vasey (2002) recorded
higher flower and young leaf intake in females during gestation and lactation, or in other words, an
increase in protein, mineral, and vitamin intake.
In order to add a nutritional dimension to this
discussion, I carried out detailed phytochemical
analyses of food plants eaten by E. mongoz, covering
water, ash, crude lipid, protein, water-soluble carbohydrates, and crude fiber. Ash can be used as an
indicator of mineral content (Lloyd et al., 1978).
Crude lipid contains triglycerides which yield energy and essential fatty acids (Lloyd et al., 1978).
Protein contents provided here are based on aminoacid analysis, and not just on the usual method of
multiplying nitrogen content by the standard conversion factor (CF) 6.25, yielding a value for crude
protein (Lloyd et al., 1978). Amino-acid analysis of
protein is preferable because the latter method is
only applicable to animal matter and leguminous
seeds, while proteins of nonleguminous plant origin
show the greatest deviation from this value (CF ⫽
5.71) (Lloyd et al., 1978; Sosulski and Imafidon,
1990). Furthermore, a large proportion of nitrogen
in plant matter is not of proteinaceous origin (20 –
65%), and is inaccessible to vertebrate digestive systems (Mossé, 1990; Lebet et al., 1994). Analysis of
water-soluble carbohydrates focused on common
sugars found in plants (glucose, fructose, and sucrose) and trehalose, which is a common sugar in
fungi. Finally, the method of determining crude fiber
content in food samples is in essence a simulation of
gastric and intestinal digestion in monogastric animals such as Eulemur sp. (Lloyd et al., 1978).
In this paper, I test the hypothesis that lemur diet
and nutrition are seasonally variable. I assess feeding behavior (time spent feeding and food items consumed), and quantify food intake and nutrient intake, in order to investigate possible links to the
evolution of small group size and female dominance
in lemurs. The mongoose lemur is an ideal candidate
for such a study, as it lives in small cohesive family
236
D.J. CURTIS
groups of 2– 6 individuals and is characterized by
female dominance (Curtis and Zaramody, 1999).
Furthermore, seasonal differences in time spent
feeding and in food items eaten are compared to
equivalent data for other Eulemur sp. My prediction
is that, although we may observe seasonal dietary
variation (food items eaten), nutrient composition
and food intake will not vary seasonally, and therefore lemurs do not suffer from seasonally induced
nutritional stress. Results obtained here on diet,
nutrition, and plant phytochemistry are also broadly
compared to information available for primates in
general. Finally, detailed information on nutrient
intake may provide valuable guidance for diets in
captivity (Curtis, 2000). In the absence of strict dietary controls, E. mongoz has in the past been particularly prone to obesity, and the precise causes of
this are as yet unknown (Clark, 1993).
METHODS
Study area and study animals
The study area was located at Anjamena (45°55⬘E;
16°03⬘S), northwestern Madagascar, in seasonally
dry, semideciduous riverine forest along the lower
reaches of the River Mahavavy. The climate was
seasonal, with 1,170 mm of the total annual rainfall
(1,190 mm) occurring during the 5-month wet season from December 1994 –April 1995. The duration
of the dry season was 7 months, lasting from May–
November. Due to the proximity of the site to the
River Mahavavy and consequent flooding, it was not
possible to work there during the peak wet season in
January and February. A map and full description of
the study site, climate, and vegetation are provided
elsewhere (Curtis and Zaramody, 1998).
E. mongoz is restricted to the seasonally dry forests of northwestern Madagascar and the Comoro
Islands (Anjouan and Mohéli) (Mittermeier et al.,
1994). It is an arboreal quadruped, socially monogamous and cathemeral, i.e. active both at night and
during the day (Curtis and Zaramody, 1999; Curtis
et al., 1999; Rasmussen, 1999; Curtis and Rasmussen, 2002). The mating season at Anjamena was in
May and June, at the beginning of the dry season,
with parturition occurring in October and November, at the end of the dry season. Lactation therefore
coincided with the end of the dry season and beginning of the wet season, and infants were weaned in
mid-wet season (Curtis and Zaramody, 1999; Curtis
et al., 2000). The two neighboring study groups
(groups 1 and 4) of mongoose lemurs were small,
cohesive family units. In September 1994, group 1
numbered 5 individuals (adult male, adult female, 2
subadult males, and juvenile female), and group 4
numbered 3 individuals (adult male, adult female,
and juvenile female). Group composition changed in
October and November 1994 during the birth season, when the adult females in both groups each
gave birth to a female infant, and between Decem-
ber–April, when the subadult males emigrated from
group 1 (Curtis and Zaramody, 1998).
Feeding behavior: data collection
The data presented here relate specifically to feeding behavior in the two study groups over 10 months
during daylight hours only, as visibility during the
nocturnal active phase of this cathemeral species
proved too limited. I conducted several short feeding
observations each month (n ⫽ 39 observations; total,
72 hr; 3–5 observations/month; 5–11 hr/month; wet
season: n ⫽ 11, 22 hr; dry season: n ⫽ 28, 50 hr;
group 1: n ⫽ 21, 41 hr; group 4: n ⫽ 18, 31 hr). These
were judged to be representative of overall feeding
behavior, as no significant difference had been found
between the amount of nocturnal and diurnal feeding behavior exhibited in the 24-hr activity budget,
and all food resources were exploited both during
the day and at night (Curtis et al., 1999).
I observed one focal animal in each observation
session, and used 15-sec instantaneous time points
to collect information on time spent feeding and
foraging (Altmann, 1974). I alternated the choice of
focal animal, with the aim of collecting representative data for each age and sex class by the end of the
study period. However, this was not achieved, and
the proportion of total feeding observation time devoted to each age and sex class was as follows: adult
male, 36% (n ⫽ 14 observations); adult female, 28%
(n ⫽ 11); subadult female, 10% (n ⫽ 5); subadult
male, 4% (n ⫽ 1); and juvenile female, 22% (n ⫽ 8).
Furthermore, sample sizes were inadequate for the
investigation of different reproductive phases (adult
female, nonreproductive: n ⫽ 3; pregnant: n ⫽ 4;
lactating: n ⫽ 4). Strict distinctions were made between “feed” and “forage,” and only activities clearly
related to food were included: “feed” was recorded
only if a food item was picked or bitten into; “forage”
was recorded if the animal was directly inspecting or
sniffing at food. To assess absolute time spent feeding, I noted the exact time at the beginning and end
of each feeding bout, which I judged to have ended
when the focal animal had exhibited no feeding behavior for more than 2 min, started feeding on something different, or moved out of the feeding tree.
Absolute counts were made of food consumed (to
establish “food intake”) by the focal animal during
each feeding bout, and plant food items were subcategorized according to van Roosmalen (1984) (Appendix). Nonplant foods included ants, spider webs,
bird’s fledglings, and earth. The term “food item”
will be used here to refer to animal matter, earth, or
the actual plant parts consumed (e.g., leaf ⫽ whole
leaf, including both the lamina and the petiole).
Chemical analysis of food items
Food sample collection and processing. All
food items eaten by the study animals were collected
during the month in which their consumption was
observed, usually on the same day I had made the
observation. Samples were generally taken from
237
DIET AND NUTRITION IN EULEMUR MONGOZ
trees in which the animals were seen feeding. If a
food source was sparsely represented within the territories of the study groups, samples were collected
from trees outside the home ranges. In total, 57 food
items were consumed during 24-hr observations
(Curtis and Zaramody, 1999; Curtis, 2000), of which
46 were available for chemical analysis. Forty-four
of these food items were eaten during the daytime
feeding observations presented here. Nectar, earth,
and animal matter were not collected.
Samples were initially processed in the field. I
collected 50 –100 g (⫾0.1 g) wet weight per food item
(electronic scales; Neolab, Zürich, Switzerland), split
every sample in half, and dried them in the sun for
up to 2 days, and then bottled samples in opaque
plastic containers each containing a small envelope
of silica gel.
Final preparations for chemical analysis were carried out in the laboratory. I discarded samples visibly contaminated by mold, and all others were
ground up using a cyclone sample mill (Cyclotec
1092, Tecator, Orpund, Switzerland), controlling for
particle size (0.5 mm) by passing the ground product
through a screen in the mill. Food items with a high
sugar content were frozen, using liquid nitrogen
prior to grinding, in order to prevent caramelization.
Chemical analysis. Water, ash, crude lipid,
crude fiber, nitrogen, amino acid, and water-soluble
carbohydrate content were determined. All samples
were analyzed in duplicate.
Water. The drying process was completed in the laboratory by heating the sample in an oven at 105°C for
3 hr (Swiss Federal Research Station for Animal Production (FAG), protocol ME103020.710).
Crude lipid. The crude lipid content was determined
by extraction, using petroleum ether (Twisselmann apparatus), followed by evaporation of the solvent
(Soxhlet apparatus), oven-drying, and gravimetric
quantification (FAG, protocol ME106010.710).
Crude fiber. Samples were washed with acetone to
remove lipids, followed by dilute acid and alkaline hydrolyses (reflux apparatus), and ignited in a muffle
furnace. The resulting weight loss is equivalent to
crude fiber content (Lloyd et al., 1978).
Ash. Samples were ignited in a muffle furnace for 4
hr at 550°C, and the weighed residue was the ash
content (FAG, protocol ME104020.710).
Water-soluble carbohydrates (fructose, glucose, sucrose, and trehalose). Extraction was carried out in
either water or aqueous ethanol (80% v/v) by heating
for 10 min at 80°C. Dichloromethane was added to
extract lipids, phases were separated by centrifugation
(2,000 rpm, 5 min), and the aqueous phase was filtered
(microfilters, 0.45 ␮m), frozen, defrosted, and centrifuged (2,000 rpm, 30 min). Sugars were quantified using high-performance liquid chromatography (HPLC;
Hewlett Packard series 1050; fructose, glucose, and
sucrose: Aminex, HPX-87P, Bio Rad, Switzerland; isocratic elution, water, 30 min, flow rate 0.6 ml/min;
trehalose: Bio-Sil Amino-5s, Bio Rad; isocratic elution,
24% MeCN in water, 25 min, flow rate 1.0 ml/min) and
a Refractive Index Detector (HP 1047A). However, only
approximate values were obtained, as the extraction
method proved unsatisfactory.
Amino acids, nitrogen, and protein. Samples were
hydrolyzed in 6 M HCl under nitrogen at 110°C for 24
hr, and amino acids were quantitated using an Alpha
Plus Amino Acid Analyzer (Pharmacia Biosystems,
Uppsala, Sweden). For tryptophan, samples were hydrolyzed in 4 M LiOH for 1 hr at 105°C and 16 hr at
120°C. A mixture of tryptophan (1 mg) and ␣-methyltryptophan (1 mg) was used as an external standard,
and ␣-methyl-tryptophan (1 mg) was used as an internal standard. HPLC (Nucleosil C18, 5 ␮l, MachereyNagel AG, Oensingen, Switzerland; isocratic elution,
1.5 g ortho-phosphoric acid and 25% MeOH in water,
pH 4; 25 min; flow rate 0.8 ml/min) and a fluorescence
detector (Hewlett Packard 1046A; wavelengths 227 nm
and 350 nm) were used to quantify tryptophan (Schneider et al., unpublished method; Institute for Food Science, ETH, Switzerland).
Nitrogen content was determined using the Dumas
method (LECO Instrumente Gmbh, Kirchheim, Germany) and converted to crude protein by multiplication
with the standard conversion factor CF ⫽ 6.25 (Lloyd
et al., 1978).
Software developed by V. Lebet (Institute for Food
Science, ETH) was used to calculate the following: true
protein (P) content based on the sum of anhydrous
amino acids (AA); the true protein conversion factor for
the sample (CFP), calculated by dividing AA by total
nitrogen recovered from the amino acids (NAA); the
crude protein conversion factor (CFCP), calculated by
dividing AA by total nitrogen content (NDumas). The
difference between CFP and CFCP permits the calculation of nonprotein nitrogen (NPN) content. The following equations were used:
冘AA
CP ⫽ 冘 N
P ⫽
anhydrous
⫻ 6.25关g/100g dry weight兴
冘AA
⫽ 冘 AA
Dumas
CF P ⫽
CF CP
关g/100g dry weight兴
冘N
/ 冘N
anhydrous
anhydrous
/
AA
Dumas
NPN ⫽ 100 ⫻ 共CF P ⫺ CF CP 兲/CF P
Chemical scores provided an estimate of protein
quality. The nutritional value of a protein depends
on the essential amino acid in greatest deficit in that
protein (the limiting amino acid), compared to a
reference protein (FAO/WHO, 1973). The chemical
score is the percentage content of the limiting amino
acid in the reference protein (Lloyd et al., 1978).
Quantification of food and nutrient intake
An estimate for food intake was calculated as follows: the mean weight of each food item was as-
238
D.J. CURTIS
sessed by weighing several representative items of
the size consumed by the animals. I then calculated
the weight ingested per food item during each observation by multiplying mean weight by number of
items, based on absolute counts made. Only the active phase of the animals’ activity was considered for
estimates of food intake, and time spent resting was
excluded. I conducted several short feeding observations each month (see Feeding Behavior: Data Collection, above). As each observation represented
only a fraction of the animal’s 24-hr activity budget,
the data had to be extrapolated from “feeding observation time” (tfo, in minutes) to “time spent active” in
the 24-hr period. I did not conduct 24-hr observations on days when feeding observations were carried out, and therefore I used “mean monthly time
spent active” (ta, in minutes), calculated based on
the data collected during the 24-hr observations in
each month (Curtis et al., 1999). This provided me
with several estimates of food intake over the 24-hr
period in each month, which was calculated as follows: I estimated daily food intake (FD) for each
24-hr period in which a feeding observation had
been made by multiplying feeding intake rate, the
weight in grams of ingested food (Ffo) divided by
“feeding observation time” (tfo), with “mean monthly
time spent active” (ta): FD ⫽ (Ffo/tfo) ta.
Daily food intake as a percentage of body weight
(FD%BW) was estimated using body weight values
collected by Pastorini et al. (1998, unpublished data)
in the study area: adult female, 1,280 g (n ⫽ 13);
adult male, 1,140 g (n ⫽ 9); subadult female, aged
21–23 months, 1,090 g (n ⫽ 4); subadult male, aged
21–23 months, 980 g (n ⫽ 2); and juvenile female,
aged 9 –11 months, 825 g (n ⫽ 2).
In a final step, I estimated daily nutrient intake
based on FD and the contents in the food samples of
water, crude ash, crude lipid, crude fiber (insoluble
carbohydrates), protein, and nonprotein nitrogenous
compounds (NPNC). NPNC contain substances that
are absorbed during digestion and are of nutritional
value (e.g., amines, vitamins, and ureides) (Sosulski
and Imafidon, 1990). Therefore, this fraction should
be included in nutritional intake, and I made a
somewhat arbitrary estimate of NPNC by treating it
as asparagine and multiplying NPN with the appropriate conversion factor (CF ⫽ 4.7) (Lloyd et al.,
1978). The fraction remaining after all other substances have been deducted from the total weight of
ingested food is the nitrogen-free extract (NFE: water-soluble carbohydrates and vitamins).
Statistical analysis
Results were summarized using descriptive statistics, and the format used for means and standard
deviations in the text and tables is mean ⫾ standard
deviation (SD). Nonparametric statistical tests were
applied, as the requirements of parametric methods
were not fulfilled and sample sizes were small (Siegel and Castellan, 1988). Standard annotation was
used for significance levels (*P ⬍ 0.05, **P ⬍ 0.01,
Fig. 1. Distribution of total observation time spent feeding on
different types of food items over entire study period.
and ***P ⬍ 0.001). Tests were carried out using
FCSTATS, version 1.1c (Wheater and Cook, 2002).
Differences in the phytochemistry of five of the
subcategories of food item (immature fruit, mature
fruit, mature seeds, immature leaves, and mature
leaves) where sample size was large enough were
investigated using a Kruskal-Wallis analysis of variance. Post hoc comparisons (Dunn’s multiple comparisons test) were carried out when statistically
significant differences were detected. Seasonal variation in nutrient content in immature and mature
fruit was assessed using a Mann-Whitney U-test.
Data from observations on the two study groups
were pooled for analysis, as food availability in both
territories was comparable and I had found no differences in the behavioral patterns exhibited by the
two groups (Curtis and Zaramody, 1998, 1999). Seasonal differences in time spent feeding and the
quantities of food items and nutrients consumed
were investigated using Wilcoxon’s signed-rank
tests. More observations were carried out during the
dry season (n ⫽ 28) than during the wet season (n ⫽
11), so dry-season observations had to be pooled in
order to carry out paired comparisons. Data for the
dry season were pooled to yield one value per group
per month for May, July, September, and November
(n ⫽ 2/month), and every other month (June, August, and October) was pooled overall (n ⫽ 1/month),
thus reducing the sample size to that of the wet
season.
RESULTS
Feeding behavior
Over the 10-month study, during the active phase
(9.6 hr; Curtis et al., 1999) of the 24-hr period, the
mean amount of time E. mongoz spent feeding accounted for 12% ⫾ 11% (1.2 hr) of observation time,
subdivided into feeding (9% ⫾ 9%) and foraging (3%
⫾ 3%). The mean value for absolute time spent
feeding (sum of feeding bouts) was higher at 21% ⫾
13%, as it included nonfeeding activities that occurred during the feeding bouts (e.g., social interac-
239
DIET AND NUTRITION IN EULEMUR MONGOZ
TABLE 1. Mean daily values ⫾ SD for total observation time (%) spent feeding on main categories of food items during dry (n ⫽
28) and wet seasons (n ⫽ 11), and test results of seasonal differences (n ⫽ 11)
Food item category
Fruit and seeds
Leaves
Flowers
Nectar
Ants
Miscellaneous
Dry season
Wet season
65 ⫾ 16
21 ⫾ 12
6⫾9
3⫾7
2⫾5
3⫾4
63 ⫾ 14
8⫾5
3⫾5
24 ⫾ 25
0
2⫾3
Wilcoxon’s signed-rank test
T⫹ ⫽ 48, T⫺ ⫽ 18;
T⫹ ⫽ 64, T⫺ ⫽ 2;
T⫹ ⫽ 10, T⫺ ⫽ 11;
T⫹ ⫽ 2, T⫺ ⫽ 26;
Only dry season
T⫹ ⫽ 25, T⫺ ⫽ 11;
P
P
P
P
⫽
⫽
⫽
⫽
0.182
0.006**
0.917
0.043*
P ⫽ 0.327
*P ⬍ 0.05
**P ⬍ 0.01
TABLE 2. Mean daily values ⫾ SD for total observation time (%) spent feeding on subcategories of food items during dry (n ⫽ 28)
and wet seasons (n ⫽ 11), and test results of seasonal differences (n ⫽ 11)
Food item subcategory
Immature fruit
Mature fruit
Seeds
Immature leaves
Mature leaves
Petioles
Immature stems
Immature flowers
Mature flowers
Nectar
Dead leaves
Dead wood
Earth
Ants
Dry season
Wet season
30 ⫾ 21
35 ⫾ 22
0.5 ⫾ 1
9⫾9
8 ⫾ 10
5⫾6
1⫾3
0
6⫾9
3⫾7
4
⬍1
⬍1
13
14 ⫾ 8
40 ⫾ 15
9 ⫾ 15
5⫾4
2⫾3
1⫾2
0
3⫾5
0
24 ⫾ 25
0
2⫾3
⬍1
0
tions or traveling). Mean duration of a feeding bout
was 2 min, 46 sec (⫾1 min, 22 sec). No differences
were observed in the amount of time spent feeding
(Wilcoxon’s signed-ranks: T⫹ ⫽ 15; T⫺ ⫽ 40; n ⫽ 11;
P ⫽ 0.202), foraging (T⫹ ⫽ 21; T⫺ ⫽ 45; n ⫽ 11; P ⫽
0.283) or in the sum of feeding bouts (T⫹ ⫽ 25; T⫺ ⫽
41; n ⫽ 11; P ⫽ 0.477) between wet and dry seasons.
Over the 10-month period, most of the observation
time was spent feeding on fruit and seeds; leaves,
flowers, nectar, ants, and miscellaneous items
(stems, dead wood, and earth) made up the remainder of the diet (Fig. 1). These broad categories were
subdivided into subcategories: most time was spent
feeding on mature fruit (37% ⫾ 20%) and immature
fruit (25% ⫾ 19%), while seeds were seldom fed on
(3% ⫾ 8%). Immature leaves (8% ⫾ 8%), mature
leaves (6% ⫾ 9%), and petioles (3% ⫾ 5%) were eaten
less frequently; mature flowers (4% ⫾ 7%) and immature flowers (1% ⫾ 3%) accounted for a small part
of feeding time; immature stems (1% ⫾ 2%) and
dead wood (1% ⫾ 2%) accounted for the largest proportion of time spent feeding on miscellaneous
items. Bird-nest predation occurred during November, but was only observed in detail once when two
fledglings were eaten by the adult female, who defended her prey aggressively and distanced herself
from other group members.
Some seasonal variation was apparent in the consumption of different categories of food items (Table
1), with leaves fed on significantly more during the
dry season, and nectar consumed predominantly
during the wet season. Animal matter (ants and
fledglings) was fed on only during the dry season. No
Wilcoxon’s signed-rank test
T⫹ ⫽ 50, T⫺ ⫽ 16;
T⫹ ⫽ 32, T⫺ ⫽ 23;
T⫹ ⫽ 1, T⫺ ⫽ 2;
T⫹ ⫽ 21, T⫺ ⫽ 7;
T⫹ ⫽ 30, T⫺ ⫽ 6;
T⫹ ⫽ 19, T⫺ ⫽ 2;
Only dry season
Only wet season
Only dry season
See Table 1
Only dry season
T⫹ ⫽ 10, T⫺ ⫽ 5;
T⫹ ⫽ 1, T⫺ ⫽ 5;
Only dry season
P
P
P
P
P
P
⫽
⫽
⫽
⫽
⫽
⫽
0.131
0.646
0.655
0.237
0.093
0.075
P ⫽ 0.500
P ⫽ 0.285
differences were found for the consumption of fruit
and seeds, flowers, or miscellaneous items. The more
detailed information on food subcategories (Table 2)
revealed no further seasonal differences.
Nutrient content of food items:
chemical analysis
The results presented here cover the basic chemical components of mongoose lemur nutrition. Detailed analytical results for each food item are given
in the Appendix, and summarized for different subcategories in Table 3.
Phytochemical differences clearly existed among
subcategories of food items consumed by the mongoose lemur (Table 3). There were statistically significant differences in water content (Kruskal-Wallis: H ⫽ 12.4; df ⫽ 4; P ⫽ 0.015), ash (H ⫽ 13.8; df ⫽
4; P ⫽ 0.008), and protein content (H ⫽ 19.2; df ⫽ 4;
P ⬍ 0.001) among the five subcategories examined
(immature and mature fruit, seeds, and immature
and mature leaves). Post hoc comparisons found significantly more water in mature and immature fruit
than in seeds, and significantly more ash in mature
leaves than in seeds, and immature leaves contained
significantly more protein than immature and mature fruit. No significant differences were found in
lipid (H ⫽ 6.9; df ⫽ 4; P ⫽ 0.142) or fiber content
(H ⫽ 5.2; df ⫽ 4; P ⫽ 0.268). Nitrogen-free extract
(NFE) was not analyzed per se, and water-soluble carbohydrates were not properly quantified; therefore,
these were excluded from statistical analysis. However, based on the approximate values obtained, mean
concentrations of water-soluble carbohydrates were
240
D.J. CURTIS
TABLE 3. Mean values for water content (% of wet weight), and lipid, fiber, ash, protein, NFE, and water-soluble carbohydrate
(glucose, fructose, sucrose, and trehalose) contents in % of dry weight1
Plant
parts
dw
fli
flm
fri
frm
ld
n
Water
Lipid
Fiber
Ash
Prot
NFE
n
Glu
Fru
Suc
Tre
1
7
1
50
6
3
39
1
0
0
0
0
1
96
1
18
5
7
62
0
1
90
1
13
7
7
70
1
ⱕ8
ⱕ10
ⱕ8
0
13
78 ⫾ 9
5⫾4
26 ⫾ 13
6⫾2
6⫾2
55 ⫾ 14
10
ⱕ2
ⱕ3
ⱕ2
0
12
78 ⫾ 8
5⫾5
26 ⫾ 12
6⫾2
5⫾2
57 ⫾ 12
11
ⱕ8
ⱕ10
ⱕ2
0
1
10
5
12
11
4
67
0
li
3
76 ⫾ 4
1 ⫾ 0.4
13 ⫾ 5
7⫾3
14 ⫾ 3
61 ⫾ 9
3
ⱕ2
ⱕ3
ⱕ2
0
lm
pm
sem
5
69 ⫾ 8
4⫾1
26 ⫾ 6
10 ⫾ 2
9⫾1
49 ⫾ 6
2
ⱕ2
ⱕ3
ⱕ2
0
2
86 ⫾ 1
2⫾1
18 ⫾ 1
18 ⫾ 2
5⫾1
56 ⫾ 2
1
ⱕ2
ⱕ3
0
0
4
47 ⫾ 23
15 ⫾ 17
15 ⫾ 20
3⫾2
9⫾3
55 ⫾ 22
3
ⱕ2
ⱕ3
ⱕ2
0
sti
2
89 ⫾ 6
2 ⫾ 0.1
25 ⫾ 17
10 ⫾ 2
9⫾4
49 ⫾ 11
1
0
0
0
0
fu
1
17
1
50
5
4
40
1
0
0
0
nq
1
i, immature; m, mature; d, dead; dw, dead wood; fl, flower; fr, fruit; l, leaf; p, petiole; se, seed; st, stem; fu, fungi; prot, protein; NFE,
nitrogen-free extract; Glu, glucose; Fru, fructose; Suc, sucrose; Tre, trehalose; nq, present but not quantifiable.
Fig. 2. Mean values for content of essential amino acids in
different food items. Trp, tryptophan; Lys, lysine; Phe, phenylalanine; Leu, leucine; Ile, isoleucine; Met, methionine; Val, valine;
Thr, threonine; i, immature; m, mature; d, dead; l, leaf; se, seed;
st, stem; fl, flower; fr, fruit; p, petiole; fu, fungi; dw, dead wood.
three times higher in mature fruit and flowers than in
any other subcategory of food item (Table 3).
In order to control for possible temporal changes
in nutrient content, immature and mature fruits
consumed during the wet and dry seasons were assessed for seasonal differences: no seasonal differences were found for immature fruit (Mann-Whitney
U-test: ash: U ⫽ 23, n ⫽ 10.3, P ⫽ 0.176; lipids: U ⫽
24, n ⫽ 10.3, P ⫽ 0.128; protein: U ⫽ 25, n ⫽ 10.3,
P ⫽ 0.091; fiber: U ⫽ 13, n ⫽ 10.3; P ⫽ 0.735; and
water: U ⫽ 26, n ⫽ 10.3, P ⫽ 0.063) or for mature
fruit (ash: U ⫽ 15, n ⫽ 4.8, P ⫽ 0.865; lipids: U ⫽ 23,
n ⫽ 4.8, P ⫽ 0.235; protein: U ⫽ 16, n ⫽ 4.8, P ⫽
1.000; fiber: U ⫽ 18, n ⫽ 4.8, P ⫽ 0.734; and water:
U ⫽ 13, n ⫽ 4.8, P ⫽ 0.610).
The total content of essential amino acids in the
different subcategories of food (Fig. 2) mirrored the
results found for protein content. Furthermore,
there were significant differences in the contents of
all essential amino acids among the five subcategories (Kruskal-Wallis: threonine: H ⫽ 18.7, df ⫽ 4,
P ⬍ 0.001; valine: H ⫽ 19.2, df ⫽ 4, P ⬍ 0.001;
methionine: H ⫽ 16.2, df ⫽ 4, P ⫽ 0.003; isoleucine:
H ⫽ 18.2, df ⫽ 4, P ⫽ 0.001; leucine: H ⫽ 20.9, df ⫽
4, P ⬍ 0.001; phenylalanine: H ⫽ 20.4, df ⫽ 4, P ⬍
0.001; lysine: H ⫽ 21.0, df ⫽ 4, P ⬍ 0.001; and
tryptophan: H ⫽ 15.0, df ⫽ 4, P ⫽ 0.005). Post hoc
comparisons found significantly more of all essential
amino acids in immature and mature leaves than in
mature fruit, with one exception: only mature leaves
contained significantly more tryptophan than mature fruit. Immature leaves contained significantly
more leucine and phenylalanine than immature
fruit. In short, out of the five subcategories investigated here, immature leaves were the richest in
essential amino acids. Chemical scores (CS) shown
in Table 4 confirm this, showing that protein quality
was highest in immature leaves (CS ⫽ 51). The
highest scores, however, were found in dead wood
and mature flowers (CS ⫽ 65 and CS ⫽ 62, respectively). The limiting amino acids in all foods were
methionine and cystine (Table 4).
Estimates of crude protein content (CP) were carried out (which includes nonproteinaceous compounds), as were the more accurate estimates of true
protein (P) based on the sum of anhydrous amino
acids in the samples. The difference between these
estimates is considerable and reflected in the differences between the two conversion factors: The true
protein conversion factor (CFP) ranged between
5.58 –5.89 (N-content, 17.9 –17.0%) for the different
food items, while the conversion factor for crude
protein (CFCP) ranged between 1.92 and 4.49 (as
opposed to the standard 6.25). The non-protein nitrogen (NPN) content ranged between 22% and 67%,
meaning that only 33–78% of nitrogen in the different food items was actually of proteinaceous origin
(Table 5).
Food and nutrient intake
Mean daily food intake (FD) for the 10-month period was estimated at 215 ⫾ 166 g (n ⫽ 39 observations). Daily food intake in percentage of body
weight (FD%BW) was estimated at 19% ⫾ 14%. No
significant seasonal differences were observed (Wilcoxon’s signed-rank test: T⫹ ⫽ 31; T⫺ ⫽ 35; n ⫽ 11;
P ⫽ 0.859; wet season: n ⫽ 11, 20% ⫾ 19%; dry
season: n ⫽ 28, 19% ⫾ 13%).
241
DIET AND NUTRITION IN EULEMUR MONGOZ
TABLE 4. Mean chemical scores and values for % deficiency of limiting amino acid in protein fraction1
Plant parts
dw
fli
flm
fri
frm
ld
li
lm
pm
sem
sti
fu
CS
Met ⫹ Cys2
65
35
44
56
62
38
49
51
41
59
43
57
51
49
45
55
47
53
43
53
48
52
47
53
1
i, immature; m, mature; d, dead; dw, dead wood; fl, flower; fr, fruit; l, leaf; p, petiole; se, seed; st, stem; fu, fungi; CS, chemical score;
Met, methionine; Cys, cystine.
2
About 75% of methionine requirement is met by cystine, based on values for humans (Lloyd et al., 1978).
TABLE 5. Comparison of mean values for crude protein and protein content in % of dry weight and
comparison of appropriate conversion factors1
Plant parts
P
CP
CFP
CFCP
NPN %
dw
fli
flm
fri
frm
ld
li
lm
pm
sem
sti
fu
3
6
5.89
2.80
52
7
16
5.68
2.58
55
7
11
5.77
3.69
36
6
9
5.66
3.83
32
5
7
5.58
3.98
29
4
6
5.79
4.09
29
14
20
5.74
4.41
23
9
13
5.84
4.49
23
5
7
5.81
3.99
31
9
13
5.67
4.42
22
9
17
5.70
3.20
44
4
13
5.74
1.92
67
1
i, immature; m, mature; d, dead; dw, dead wood; fl, flower; fr, fruit; l, leaf; p, petiole; se, seed; st, stem; fu, fungi; CF, conversion factor;
P, protein; CP, crude protein; NPN, nonprotein nitrogen.
Fig. 3. Distribution of nutrient intake, excluding water, over
entire study period. NPNC, nonprotein nitrogenous compounds;
NFE, nitrogen-free extract.
The main constituent in food consumed throughout the study period was water (81%). Fiber and
nitrogen-free extract (NFE) accounted for more than
80% of dry substance, while ash, lipids, protein, and
digestible nonprotein nitrogenous compounds
(NPNC) were consumed in smaller quantities (Fig.
3). No significant seasonal differences were found in
estimated nutrient intake (Table 6). Likewise, no
variation was apparent in the intake of essential
amino acids between wet and dry seasons (Table 7).
DISCUSSION
Seasonal variation in feeding behavior
Time spent feeding in the mongoose lemur both at
Anjamena and at Ampijoroa (Curtis and Zaramody,
1999; Rasmussen, 1999), 6% and 9%, respectively, is
at the low end of the range reported for other Eulemur species studied during all seasons (12–22%)
(Sussman, 1974; Overdorff, 1993; Tattersall, 1977;
Rasmussen, 1999; Vasey, 2002). The reason for this
discrepancy may well be that most available data for
Eulemur sp. stem from observations conducted dur-
ing daytime only. Given the seasonal variability in
the amount of nocturnal activity exhibited by these
cathemeral species, this could result in an over- or
underestimation of time spent feeding (Curtis and
Rasmussen, 2002). Observations on the mongoose
lemur were carried out throughout the 24-hr period,
and neither study found any difference in time spent
feeding between nocturnal and diurnal activity
(Curtis et al., 1999; Rasmussen, 1999). In spite of
this, most studies on Eulemur sp. reveal no significant seasonal differences in time spent feeding, as is
the case for the mongoose lemur at Anjamena.
The mongoose lemur conforms to the general dietary pattern for Eulemur sp., which is predominantly frugivorous, supplemented to varying degrees by leaves, flowers, and nectar (Sussman, 1974;
Tattersall, 1977; Overdorff, 1993; Freed, 1996;
Colquhoun, 1997; Vasey, 2002; Andrews and Birkinshaw, 1998; Donati et al., 1999; Rasmussen, 1999).
Because of the high dependence on fruit in Eulemur
sp., discussion of seasonal dietary variability has
usually focused on periods of fruit scarcity and/or
the dry season. However, there are habitat-dependent differences in the extent of frugivory and how
this diet is supplemented by other foods. A comparison of Eulemur diets reveals a high reliance on fruit
during all seasons in coastal and montane rainforests throughout Madagascar (Overdorff, 1993;
Freed, 1996; Andrews and Birkinshaw, 1998; Vasey,
2002). In the East, there is an actual increase in
frugivory during periods of fruit scarcity (Overdorff,
1993; Vasey, 2002), varying amounts of flower, leaf,
and nectar consumption during all seasons in montane rainforest (Overdorff, 1993), and a peak in leaf
and flower consumption during the hot season when
food is abundant in the coastal rainforest (Vasey,
2002). In western rainforest there is an increase in
flower, nectar, or leaf consumption during the dry
season (Freed, 1996; Andrews and Birkinshaw,
1998). In the seasonal forests of the Comorian island
Mayotte and in western Madagascar, fruit did not
242
D.J. CURTIS
TABLE 6. Mean values for nutrient intake in % of body weight during dry (n ⫽ 28) and wet seasons (n ⫽ 11),
and test results of seasonal differences (n ⫽ 11)1
Nutrient categories
Water
Ash
Crude lipid
Protein
NPNC
Crude fiber
NFE
1
Dry season
Wet season
15.48 ⫾ 10.79
0.24 ⫾ 0.14
0.07 ⫾ 0.07
0.18 ⫾ 0.13
0.08 ⫾ 0.05
0.60 ⫾ 0.54
2.17 ⫾ 1.46
16.30 ⫾ 16.52
0.25 ⫾ 0.21
0.24 ⫾ 0.29
0.22 ⫾ 0.18
0.06 ⫾ 0.05
1.06 ⫾ 0.91
2.23 ⫾ 1.76
Wilcoxon’s signed-rank test
T⫹
T⫹
T⫹
T⫹
T⫹
T⫹
T⫹
⫽
⫽
⫽
⫽
⫽
⫽
⫽
32,
35,
54,
43,
12,
48,
33,
T⫺
T⫺
T⫺
T⫺
T⫺
T⫺
T⫺
⫽
⫽
⫽
⫽
⫽
⫽
⫽
34;
31;
12;
23;
33;
19;
33;
P
P
P
P
P
P
P
⫽
⫽
⫽
⫽
⫽
⫽
⫽
0.929
0.859
0.062
0.374
0.212
0.197
1.000
NPNC, nonprotein nitrogenous compounds; NFE, nitrogen-free extract.
TABLE 7. Mean values for intake of essential amino acids in % of body weight during dry (n ⫽ 28) and wet seasons
(n ⫽ 11), and test results of seasonal differences (n ⫽ 11)
Essential amino acid
Threonine
Valine
Methionine
Isoleucine
Leucine
Phenylalanine
Lysine
Tryptophan
Dry season
Wet season
0.008 ⫾ 0.007
0.010 ⫾ 0.008
0.003 ⫾ 0.002
0.008 ⫾ 0.007
0.014 ⫾ 0.010
0.009 ⫾ 0.008
0.010 ⫾ 0.008
0.003 ⫾ 0.002
0.013 ⫾ 0.012
0.014 ⫾ 0.014
0.003 ⫾ 0.003
0.012 ⫾ 0.013
0.019 ⫾ 0.018
0.015 ⫾ 0.016
0.015 ⫾ 0.015
0.005 ⫾ 0.005
feature quite as prominently in the diet. There was
a shift towards increased folivory, and consumption
of flowers, nectar, and pollen during the dry season,
but these food items were also important during the
wet season (Sussman, 1974; Tattersall, 1977; Andriatsarafara, 1988; Colquhoun, 1997; Donati et al.,
1999; Rasmussen, 1999; Curtis, 2000). At Anjamena
the mongoose lemur spent significantly more time
feeding on leaves during the dry season, animal
matter was fed on only during the dry season, and
nectar consumption was significantly greater during
the wet season. This comparison reveals a relatively
high variability in dietary strategies in this group of
closely related lemurs, mirrored in the home-range
sizes, which are larger in the East than in the West
and indicate that Eulemur sp. need to range further
in the East to find the necessary resources (Curtis
and Zaramody, 1998). The observed variability is
probably related to differences in food availability
and food quality in the various types of habitat.
Fruit is regarded as rich in carbohydrates and lipids,
nectar as rich in carbohydrates, and leaves, flowers,
and seeds as the main source of protein, minerals,
and most vitamins. Digestibility of leaves and flowers is viewed as low due to high fiber content (Waterman, 1984), although both immature and mature
tropical fruit were found to contain levels of fiber as
high as those in foliage (e.g., Remis et al., 2001).
Based on long-term data from Kirindy in the
West, fruit is available year-round and is a predictable resource in these seasonally dry forests. However, fruit available during the dry season is fibrous,
with little or no flesh and lower quality than fruit
available during the wet season (Ganzhorn et al.,
1999). At Anjamena, almost half of the fruit consumed by E. mongoz during the dry season was
immature and probably contained high levels of di-
Wilcoxon’s signed-rank test
T⫹
T⫹
T⫹
T⫹
T⫹
T⫹
T⫹
T⫹
⫽
⫽
⫽
⫽
⫽
⫽
⫽
⫽
46,
46,
23,
31,
38,
39,
35,
32,
T⫺
T⫺
T⫺
T⫺
T⫺
T⫺
T⫺
T⫺
⫽
⫽
⫽
⫽
⫽
⫽
⫽
⫽
20;
21;
13;
15;
18;
16;
20;
14;
P
P
P
P
P
P
P
P
⫽
⫽
⫽
⫽
⫽
⫽
⫽
⫽
0.247
0.266
0.481
0.343
0.307
0.241
0.445
0.286
gestion-inhibiting or toxic compounds (Waterman,
1984), and therefore may well have constituted a
low-quality resource. Crude fiber content did not
differ significantly between fruit and leaves, and
high levels of fiber were found in both immature and
mature fruit consumed by E. mongoz. However, no
seasonal differences were found in nutrient content
(ash, lipids, protein, fiber, and water) between mature or immature fruit consumed during the wet
season, when compared to the dry season. Differences in water-soluble carbohydrate levels could not
be assessed, as only approximate values were obtained, but the lack of seasonal differences in water
content indicates that there was no difference in
how fleshy fruits were between the wet and dry
season. The absence of seasonal differences in nutrient content in fruit might explain the increased time
spent feeding on foods other than fruit during both
the wet and the dry seasons in the West when compared to rainforest habitat, with the lemurs relying
less on fruit, a predictable but possibly lower-quality
resource. At Anjamena, seeds and mature flowers
were a source of carbohydrates, lipids, protein, and
minerals during both seasons; nectar was an important source of carbohydrates during the wet season;
and leaves and animal matter constituted an important source of protein and minerals during the dry
season.
Long-term data from rainforest habitat at Ranomafana in the East revealed that fruit production is
seasonally variable, and its availability is unpredictable from one year to the next, but there is a yearround supply of fleshy fruit (Ganzhorn et al., 1999).
The frequent impact of cyclones, combined with occasional frost in some areas and low soil fertility in
the East, may well be the reasons for this unpredictability (e.g., Overdorff, 1993; Ganzhorn et al., 1999;
DIET AND NUTRITION IN EULEMUR MONGOZ
Wright, 1999). If high-quality fleshy fruit is available during all seasons in the East, then it may be
possible for Eulemur sp. to rely on this resource to a
greater extent, and increase time spent foraging for
fruit during periods of fruit scarcity, as observed by
Overdorff (1993) and Vasey (2002). However, unpredictability can result in migration to other areas
during serious shortages, as was documented for E.
fulvus rufus at Ranomafana. Year-round reliance on
fruit is almost as high in the northwestern rainforest, which may mean that higher-quality fruit is
available in all types of rainforest. Conversely, the
increase in flower, nectar, or leaf consumption during the dry season in northwestern rainforest could
indicate that fruit quality is low in all western forests during the dry season.
Food and nutrient intake
In accordance with my prediction, no significant
seasonal variation was observed in the estimates for
daily food intake or nutrient intake. Although my
database is small, this indicates that the available
food resources are exploited such that nutrient requirements are met during both the wet and dry
seasons. There is no indication that food resources
are maximally exploited during periods of abundance in order to build up reserves to tide over
periods of scarcity, or that seasonality leads to periods of nutritional stress (King and Murphy, 1985;
Pereira et al., 1999; Wright, 1999). However, we
require more detailed studies on a variety of species
assessing food and nutrient intake. We also need
more information on behavioral, anatomical, and in
particular, physiological mechanisms before we can
be sure that nutrition is adequate throughout the
year. Below, I compare the data presented here for
E. mongoz with what little information is available
on other primates in terms of food and nutrient
intake, and nutrient requirements.
Daily food intake by E. mongoz in percentage of
body weight (19%) was comparable to that observed
in other primates (Alouatta, 15%; Cebus, 13%; and
Gorilla, 20%) (Hladik et al., 1971; Goodall, 1977, in
Richard, 1985; Chamberlain et al., 1993). Water requirements would have been adequately covered, as
average daily water intake in percentage of body
weight was 16% (ca. 160 g/kg body weight), and was
complemented by licking dew off leaves and obtaining water from tree hollows.
At approximately 2.2 g/kg body weight, average
protein intake was higher than the recommended
daily requirements for adult humans of 0.8 g/kg
body weight (Lloyd et al., 1978), but lower than
recommendations for macaques (3 g/kg body weight)
(Portman, 1970). The average daily intake of essential amino acids exhibited little deviation throughout the study period. Comparison with the requirements for adult humans revealed consistently lower
intakes, varying between 14 –25% of recommended
intakes for all amino acids except methionine, which
was even lower (5%) (Lloyd et al., 1978). Comparison
243
with available data from other studies on nonhuman
primates covering a range of diets and dietary specializations (cebids, callitrichids, colobines, cercopithecines, pongids, and lemurs) showed that the
dietary intake of protein appears to be at the low end
of the range (6% of dry weight in E. mongoz, compared to a range of 7–21%) (Coelho et al., 1976;
Hladik, 1978; Richard, 1985; Barton et al., 1993;
Chamberlain et al., 1993; Sterling et al., 1994; Conklin-Brittain et al., 1998). However, the methodology used here aimed at providing an estimate of true
protein intake (based on total amino-acid intake).
Most other studies used crude protein, which yields
higher estimates (Sosulski and Imafidon, 1990; Lebet et al., 1994) and overestimates protein intake.
Furthermore, bird-nest predation occurred during
November, while the adult females were lactating,
and would have constituted a source of additional
protein during the early phases of lactation (Portman, 1970; Lloyd et al., 1978). Predation on birds
and eggs was reported for E. fulvus sp. in captivity
(Glander et al., 1985; Shedd, 1990), as well as for E.
f. fulvus at Ampijoroa (U. Thalmann, personal communication), suggesting that this is a part of normal
foraging behavior in the genus Eulemur.
Crude lipid intake averaged 3% of dry weight, and
is at the low end of the range found in other studies
(range, 3–16%; Daubentonia, 43%) (Coelho et al.,
1976; Hladik, 1978; Richard, 1985; Barton et al.,
1993; Chamberlain et al., 1993; Sterling et al., 1994;
Conklin-Brittain et al., 1998). The low lipid intake
observed in E. mongoz in combination with its physiology, i.e., in all probability a low basal metabolic
rate (Müller, 1983; Daniels, 1984), may provide an
indication as to why this species exhibited a tendency to obesity in captivity in the past (Clark, 1993)
when fed an inappropriate diet.
Crude fiber intake (21% of dry weight) is extraordinarily high, given the fact that this species has a
short gut passage rate, and its gut morphology is not
equipped to deal with a high-fiber diet (Overdorff
and Rasmussen, 1995; Lambert, 1998). Both immature and mature fruit consumed by E. mongoz contained high levels of fiber, and no seasonal differences were apparent in fruit quality. Given the
relatively short gut passage rate time in E. mongoz,
low-quality mature fruit as well as immature fruit
may be eaten in order to gain access to water and
readily digested components, while the fibrous component is rapidly expelled (Davies et al., 1988). Comparative data for Alouatta, Ateles, Cebus, and Saguinus found a decrease in crude fiber intake from
mainly folivorous, through frugivorous, to insectivorous species (14% to 7%) (Hladik et al., 1971), and
Chamberlain et al. (1993) found that crude fiber
intake made up 44% of daily dry mass consumption
for Alouatta. The high fiber intake documented here
for E. mongoz ranks with that observed for folivorous species, and should perhaps also be taken into
account in captive diets.
244
D.J. CURTIS
Comparison of other nutrient intakes was not possible due to a lack of comparable information and
differences in analytical methods.
Finally, geophagy and the consumption of dead
wood occurred regularly throughout the entire year.
The mechanical and pharmaceutical properties of
soil could aid in detoxification (Johns and Duquette,
1991; Knezevich, 1998; Krishnamani and Mahaney,
2000) of the immature fruit that were consumed,
which are thought to contain high levels of toxins
and digestion inhibitors (Waterman, 1984). Soil consumption might also counteract the effects of parasitosis (Johns and Duquette, 1991; Knezevich, 1998;
Krishnamani and Mahaney, 2000): parasitic nematodes were frequently observed in feces.
Seasonality, female dominance, and small
group size in lemurs
The “energy conservation hypothesis” proposes
that female dominance and small group size have
allowed lemurs to cope with strong seasonality in
Madagascar and the resulting scarcity of important
food resources, and to avoid energetic stress during
gestation and lactation, when the energy requirements of females are high (Jolly, 1984; Richard and
Nicoll, 1987; Meyers and Wright, 1993; Young et al.,
1990; Pereira et al., 1999). Wright (1999) took this
further in the “energy frugality hypothesis,” postulating that these and other behavioral adaptations
serve not only to conserve energy during gestation
and lactation, but also to maximize the use of scarce
resources. An example of this is the synchronization
of weaning with food abundance, which may ensure
maximum survival rates for offspring. Eulemur sp.
are predominantly frugivorous, and therefore the
main food resource has usually been regarded as
fruit, although it was more recently suggested that
the overall diversification of the diet and increased
consumption of leaves and flowers during gestation
and lactation may be important (Pereira et al., 1999;
Vasey, 2002).
Data on seasonal dietary variation in the mongoose lemur appear to largely agree with these hypotheses. During the dry season, which coincides
with gestation and much of lactation, more items
regarded as low-energy foods are eaten, and the
overall digestibility of food appears lower (leaves,
immature fruit, and stems). The diet is more diverse
and protein, vitamin, and mineral intake is possibly
higher. During the wet season, which coincides with
the end of lactation and weaning, 64% of feeding
time is spent on mature fruit and nectar, which are
regarded as high-energy foods (carbohydrates and
lipids). Nectar is easily digestible.
Phytochemical analyses and the estimates of nutrient intake reveal a different picture. The diet is
characterized by low digestibility during both seasons, as both immature and mature fruit exhibited
high fiber contents. Based on behavioral feeding
data alone, we would predict that the increase in
folivory during the dry season would result in an
increase in fiber intake, as well as an increase in the
volume of food ingested and therefore in food intake
in percentage of body weight (e.g., Hladik et al.,
1971). However, no seasonal differences were observed in food intake in percentage of body weight.
Nutrient intake was also stable across both seasons
and exhibited little variability at all, indicating that
more caution is needed when interpreting information on dietary variability between seasons in the
absence of phytochemical analyses.
The phytochemical and nutritional data provided
here for E. mongoz do not support the hypotheses
that energy must be conserved during the dry season (gestation and lactation), or that the use of highenergy resources is maximized during the wet season (weaning), as no seasonal variability is observed
in nutritional intake. However, analysis of watersoluble carbohydrates, one high-energy source,
yielded only approximate values. These conclusions
are based on a small and incomplete body of data,
and therefore must be regarded as preliminary, and
should be investigated in more comprehensive studies. Furthermore, different reproductive phases and
intersexual variation need to be assessed in detail in
order to provide conclusive evidence that female
dominance and small group size are not connected to
seasonal differences in nutrient and energy availability. However, this investigation does indicate
that nutritional demands are probably adequately
fulfilled during both seasons, and that mongoose
lemurs do not suffer from nutritional stress (King
and Murphy, 1985; Pereira et al., 1999).
ACKNOWLEDGMENTS
I am indebted to R.D. Martin for his academic
guidance and to U. Thalmann, whose hard work
provided the logistic basis without which the
present study might never have been carried out.
Field work was conducted under an Accord de Coopération between the Universities of Zürich (Switzerland) and Mahajanga (Madagascar), and research permission was provided by Malagasy
governmental organizations. I thank the staff at the
University of Mahajanga, in particular A. Zaramody, for their assistance at various stages during
the field work, and J. Raharilala at the Parc Botanique et Zoologique Tsimbazaza for plant determination. For additional assistance in field work, I am
grateful to the following people: A. Blaise, M.-E.
Blaise, P. Müller, O.D. Rabetsimialona, E.O. Raheliarisoa, A. Velo, and many of the local inhabitants
in Anjamena and Mitsinjo. Thanks go to T. Rihs at
the Swiss Federal Research Station for Animal Production (FAG, Posieux, Switzerland), to R. Amadò,
G.G.G. Manzardo, S. Farahi-Shad, S. Kürsteiner, Q.
Luethi-Peng, H. Schneider, and B. Staufer at the
Institute for Animal Nutrition, and to A. Gutknecht
at the Institute for Food Science (ETH Zürich, Switzerland) for their guidance and assistance in the
laboratory and in some cases the chemical analyses
they carried out for me. D. Glaser kindly provided
245
DIET AND NUTRITION IN EULEMUR MONGOZ
APPENDIX. Results of nutritional analysis for plant species fed on according to plant part in % of dry weight,
excepting water (in % of fresh weight)1
Plant family
Apocynaceae
Borraginaceae
Plant species
Landolphia perrieri
Cordia subcordata
Ehretia sp.
Caesalpiniaceae
Cordia sp.
Tamarindus indica
Combretaceae
Poivrea obscura
Flagellariaceae
Terminalia mantaly
Argyreia sp.
Diospyros
megasepala
Phyllanthus sp.
Antidesma petiolare
Flagellaria indica
Leeaceae
Moraceae
Leea guineensis
Ficus cocculifolia
Convolvulaceae
Ebenaceae
Euphorbiaceae
Papilionaceae
Passifloraceae
Rhamnaceae
Rubiaceae
Ficus soroceoides
Bosqueia sp.
Rhynchosia bauckea
Mucuna pruriens
Passiflora foetida
Zizyphus jujuba
Violaceae
Vitaceae
Paeoleria farinosa
Tricalysia sp.
Paullinia pinnata
?
Grewia sp.
Grewia
lavanalensis
Rinorea sp.
Cissus sp.
Not determined
Not determined
Sapindaceae
Sterculiaceae
Tiliaceae
Plant
part
Ash
Lipids
Nitrogen
Protein
(AAA)
NPNC
Fiber
NFE
Glu
Fru
Suc
Water
fr/i
l/m
p/m
fr/m
fr/i
fr/m
se/m
se/m
l/i
l/m
fr/i
fr/i
st/i
fr/i
fr/m
l/m
2.9
7.8
16.8
5.3
6.0
4.5
6.2
2.3
4.1
10.5
3.6
6.6
8.3
3.3
8.7
10.4
5.0
4.7
1.4
1.1
10.1
5.4
7.5
3.3
1.1
4.0
0.9
6.4
1.7
0.2
2.7
3.8
0.6
1.5
1.4
0.9
1.9
1.5
2.0
2.0
3.2
2.1
0.9
3.1
1.1
2.3
2.3
2.2
2.3
7.1
5.4
2.3
6.3
4.8
6.4
10.8
13.2
9.2
3.7
9.7
6.1
3.5
9.8
9.2
0.9
1.4
2.3
2.3
3.8
3.0
3.9
0.5
4.2
2.3
1.1
6.6
5.7
2.2
3.1
2.8
2.0
28.2
16.9
21.1
37.2
37.1
44.5
8.7
7.4
23.5
39.0
27.7
37.2
42.1
13.3
25.6
86.9
50.7
57.3
67.9
36.6
45.2
31.6
74.4
70.0
50.4
51.7
43.1
41.1
48.7
62.4
48.2
ⱕ8.3
n.d.
ⱕ2.1
ⱕ8.3
0.0
ⱕ2.1
ⱕ2.1
n.d.
ⱕ2.1
ⱕ2.1
n.d.
ⱕ2.1
n.d.
0.0
ⱕ8.3
n.d.
ⱕ10.0
n.d.
ⱕ2.5
ⱕ10.0
0.0
ⱕ2.5
ⱕ2.5
n.d.
ⱕ2.5
0.0
n.d.
ⱕ2.5
n.d.
0.0
0.0
n.d.
ⱕ2.1
n.d.
0.0
ⱖ8.3
0.0
0.0
ⱕ2.1
n.d.
ⱕ2.1
0.0
n.d.
ⱕ2.1
n.d.
0.0
0.0
n.d.
59.1
66.3
86.1
72.0
70.4
77.7
68.7
14.6
81.2
72.3
79.6
82.9
84.4
77.3
87.7
59.4
fr/i
fr/m
l/m
fr/i
fr/m
fr/m
fr/i
l/i
p/m
fr/i
se/m
fl/m
fl/i
fr/m
fr/m
dw
l/i
fr/i
st/i
l/m
fr/m
se/m
fr/i
fr/m
fr/m
5.5
4.4
9.2
6.4
4.7
9.2
8.3
10.1
19.9
10.5
2.3
6.9
5.4
5.4
7.7
5.8
6.7
6.6
11.4
13.9
4.8
2.8
4.8
9.3
5.6
5.2
3.8
2.5
1.5
20.3
5.1
3.1
1.8
2.7
7.9
9.7
1.0
1.1
2.2
0.9
0.8
1.4
0.5
1.8
3.3
2.1
39.9
1.0
3.0
4.5
1.8
0.7
2.5
1.5
0.9
0.9
1.6
2.3
0.9
n.d.
2.2
1.8
2.5
1.3
0.8
1.0
4.0
1.5
3.3
1.9
1.1
2.0
1.1
1.3
1.1
7.5
2.7
10.7
5.8
4.1
3.8
6.8
10.8
3.7
8.8
12.8
6.5
6.5
6.8
2.3
2.7
17.6
5.8
20.5
9.2
4.2
6.7
3.9
5.2
5.0
2.4
1.0
3.4
2.9
0.8
1.0
2.0
1.9
1.3
n.d.
0.3
3.0
6.5
0.1
2.0
2.4
4.6
2.4
12.2
1.5
1.6
3.7
1.6
2.0
1.1
21.0
24.6
34.0
12.6
21.6
21.5
25.6
13.9
18.5
18.1
2.1
12.6
18.4
29.5
3.4
49.5
18.0
12.6
12.9
16.9
40.5
6.2
45.1
37.0
42.0
58.4
63.6
40.2
70.8
48.5
59.4
54.2
61.5
53.8
54.7
72.9
70.0
62.1
56.0
83.7
38.8
51.7
72.1
56.2
55.2
46.7
40.7
43.6
43.5
41.8
ⱕ2.1
ⱖ8.3
ⱕ2.1
ⱕ2.1
ⱕ8.3
ⱕ8.3
ⱕ8.3
0.0
n.d.
ⱕ2.1
0.0
ⱕ8.3
n.d.
ⱕ8.3
ⱖ8.3
0.0
ⱕ2.1
n.d.
n.d.
n.d.
ⱕ2.1
ⱕ8.3
n.d.
n.d.
ⱕ2.1
ⱕ2.5
ⱖ10.0
ⱕ2.5
ⱕ2.5
ⱕ10.0
ⱕ10.0
ⱕ10.0
0.0
n.d.
ⱕ2.5
0.0
ⱕ10.0
n.d.
ⱕ10.0
ⱖ10.0
0.0
ⱕ2.5
n.d.
n.d.
n.d.
ⱕ2.5
ⱕ10.0
n.d.
n.d.
ⱕ2.5
ⱕ2.1
0.0
ⱕ8.3
ⱖ8.3
ⱕ2.1
ⱕ2.1
ⱕ2.1
0.0
n.d.
0.0
ⱕ2.1
ⱖ8.3
n.d.
0.0
0.0
0.0
ⱕ2.1
n.d.
n.d.
n.d.
0.0
ⱕ8.3
n.d.
n.d.
0.0
81.4
84.3
68.4
69.1
74.9
91.5
88.7
73.6
84.9
88.7
53.1
89.6
96.2
81.6
83.2
6.6
73.7
88.3
93.3
79.9
74.2
51.6
69.8
83.5
65.4
fr/i
fr/i
fr/m
l/d
fu
5.3
4.4
2.9
10.9
5.3
5.2
11.7
7.4
4.9
1.0
1.3
1.4
1.2
1.0
2.0
4.7
6.7
6.4
4.0
3.9
2.0
1.0
0.3
1.4
6.4
25.9
33.3
18.3
12.2
49.5
56.9
42.9
64.7
66.7
33.9
ⱕ8.3
ⱕ2.1
ⱕ8.3
n.d.
0.0
ⱖ10.0
0.0
ⱕ10.0
n.d.
0.0
ⱕ2.1
0.0
ⱕ8.3
n.d.
0.0
78.7
78.9
65.8
10.4
16.7
1
l, leaf; fr, fruit; se, seed; p, petiole; st, stem; fl, flower; n, nectar; dw, dead wood; fu, fungus; i, immature; m, mature; d, dead; AAA,
amino-acid analysis; NPNC, nonprotein nitrogen content; NFE, nitrogen-free extract; Glu, glucose; Fru, fructose; Suc, sucrose.
Standard error (SE) or standard deviation (SD) for different analyses: ash: SE ⫽ 0.6%; lipids, SE ⫽ 1.1%; nitrogen, SD ⱕ5%, excepting
Cordia subcordata p/m (SD ⫽ 21%); protein, SD ⱕ5%, excepting Mucuna pruriens fl/i (SD ⫽ 9%); fiber, SD ⱕ5%, excepting Cordia
subcordata fr/m (SD ⫽ 6%) and Passiflora foeotida fr/m (SD ⫽ 6%); water, SD ⫽ 5%. Results for trehalose are all 0.0% excepting
fungus, where trehalose is present, but not quantified.
contacts for the analytical work. I also thank C. Ross
and two anonymous reviewers for their invaluable
comments on the manuscript. Financial support was
provided by the A.H. Schultz-Stiftung, G. & A.
Claraz-Schenkung, Goethe Stiftung, Schweizerische
Akademie der Naturwissenschaften, Primate Conservation, Inc., and an EU project, “The Mechanistic
Understanding of the Sweetness Response” (AIR3CT94-2107), funded by a grant awarded to D. Glaser
by the Bundesamt für Bildung und Wissenschaft
(BBW 94.0156), Bern, Switzerland.
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implications, mongoose, diet, lemur, group, dominance, evolution, small, wild, eulemur, female, size, mongoz, nutrition
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