Diet and nutrition in wild mongoose lemurs (Eulemur mongoz) and their implications for the evolution of female dominance and small group size in lemurs.код для вставкиСкачать
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: firstname.lastname@example.org 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. LITERATURE CITED Altmann J. 1974. 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