feeding patterns and dietary profile of nocturnal southern woolly lemurs (avahi meridionalis) in...

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International Journal of PrimatologyThe Official Journal of the InternationalPrimatological Society ISSN 0164-0291Volume 33Number 1 Int J Primatol (2012) 33:150-167DOI 10.1007/s10764-011-9562-3

Feeding Patterns and Dietary Profile ofNocturnal Southern Woolly Lemurs (Avahimeridionalis) in Southeast Madagascar

Ivan Norscia, Jean BaptisteRamanamanjato & Jörg U. Ganzhorn

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Feeding Patterns and Dietary Profileof Nocturnal Southern Woolly Lemurs(Avahi meridionalis) in Southeast Madagascar

Ivan Norscia & Jean Baptiste Ramanamanjato &

Jörg U. Ganzhorn

Received: 24 August 2011 /Accepted: 2 September 2011 /Published online: 2 December 2011# Springer Science+Business Media, LLC 2011

Abstract Folivory has evolved in all primate radiations but the relative importanceof resource quantity and nutritional quality of food is controversial. To understandhow food abundance and different nutrients affect a folivorous diet, we investigatedfood composition of the leaf-eating lemur Avahi meridionalis. From June toDecember 2004, we conducted 26 nights of focal observation (256.1 h) in SainteLuce pluvial littoral forest (southeast Madagascar) and recorded feeding behavior of4 radiocollared individuals. Within the subjects’ home ranges, we recordedvegetation characteristics (morphospecies, phenology, diameter at breast height)and sampled food and nonfood items for chemical analyses. A. meridionalis did noteat fruit but only leaves and flowers and did not base their choice on foodabundance. Adult leaves eaten were higher in easily soluble protein than adult leavesthat were not consumed. The subjects ate young leaves and flowers as soon as theybecame available. These young leaves contained the same concentrations of solubleprotein, higher concentrations of crude protein, and lower concentrations of aciddetergent fiber and sugar than mature food leaves. A. meridionalis ate leaves withcondensed tannins, alkaloids, and intermediate concentrations of polyphenolics. Contraryto previous studies that considered Avahi spp. a specialist, A. meridionalis acted as leaf-eating generalists with moderate selectivity, based on nutritional quality and tolerance ofa wide array of plant secondary metabolites. This illustrates the dietary flexibility withina single genus of primates that seems to be driven by environmental constraints ratherthan morphological or physiological adaptations.

Int J Primatol (2012) 33:150–167DOI 10.1007/s10764-011-9562-3

I. NorsciaMuseo di Storia Naturale e del Territorio, Università di Pisa,56011 Calci, Pisa, Italye-mail: [email protected]

J. B. RamanamanjatoQIT Madagascar Minerals SA, BP 614 Tolagnaro, Madagascar

J. U. Ganzhorn (*)Abt. Tierökologie und Naturschutz, Universität Hamburg, 20146 Hamburg, Germanye-mail: [email protected]

Author's personal copy

Keywords Alkaloids . Fiber . Folivory . Polyphenolics . Primates . Protein . Tannins

Introduction

Herbivores can be assigned to generalists, which eat a wide array of plant species, andspecialists, which feed on 1 or a few closely related plants (Dearing et al. 2000;Freeland 1991). These categories are likely to be flexible (Shipley et al. 2009), as eventhe most specialized mammalian herbivores, such as koalas (Phascolarctos cinereus),can consume 120 species in the genus Eucalyptus and 30 noneucalypt species (Mooreand Foley 2000). At the other end of the scale, generalist herbivores, such as hyraxes(Heterohyrax brucei and Procavia johnstoni: Hoeck 1989) can reduce their dietaryrange in case of increased interspecific competition over food. Bamboo lemurs(Hapalemur spp.), considered bamboo specialists, can vary their diets in relation tohabitat characteristics in a way that justifies their classification as generalists (Eppleyet al. 2011; Grassi 2006; Mutschler 1999; Tan 1999; Yamashita et al. 2010). Similarly,desert woodrats (Neotoma lepida) can be classified either as specialists (Dial 1988) oras generalists (Skopec et al. 2008) with dietary variability among populations.

Folivory occurs in all primate radiations (Fleagle 1998). Owing to the sometimeslow nutritional quality of leaves, the difficulty of digesting fiber, and thepresence of potentially toxic secondary compounds (Glander 1982; Milton 1979),the evolutionary constraints imposed by leaf eating have remained issues in nutritionalecology. These studies focus on 2 trade-offs: that between food abundance and dietarychoice and that between generalized and specialized diets.

Food Abundance or Dietary Choice

Leaves are bulky, often low-quality food and folivores need to ingest large amounts tosatisfy their nutritional requirements. On the one hand, animals should select high-quality leaves to reduce the biomass ingested and facilitate digestibility because their gutcapacity is limited. On the other hand, high selectivity is likely to require longer distancetravel between suitable food patches. Therefore selectivity is likely to increase searchtime and associated energy demands. Feeding on items according to their availabilitywould reduce these additional travel costs and conserve energy. This trade-off has beensubject to several investigations (Duncan and Gordon 1999; Westoby 1974). Somefolivorous primates ingest food mainly in relation to its availability, e.g., Alouattacaraya (Bicca-Marques and Calegaro-Marques 1994), Alouatta pigra (Pavelka andKnopff 2004), and Presbytis melalophus (Johns 1986), whereas others appear to bemore influenced by food quality, e.g., Lepilemur ruficaudatus (Ganzhorn 2002), Asiancolobines (Yeager and Kirkpatrick 1998), and African colobines (Chapman et al.2002, 2004; Oates et al. 1990). The trade-off between energy/nutrient maximizationand time minimization can vary seasonally (Hemingway and Bynum 2005).

Diet Breadth: Generalized or Specialized Diets

Diet breadth can be related to plant primary or secondary metabolites. For primarymetabolites, the nutrient constraint hypothesis proposes that dietary specialization in

Nutritional Ecology of Avahi meridionalis 151


mammalian herbivores is rare because single plant species are unlikely to satisfy allnutritional demands of a herbivore (Freeland and Janzen 1974; Wiggins et al. 2006).Two important leaf components for folivores are proteins, crucial for bodilyfunctions, and fiber, which slows digesta passage rate and reduces digestiveefficiency (Demment and van Soest 1985; Mackie 2002; Milton 1979). Twohypotheses stress the pivotal role of proteins: The protein maximization hypothesissuggests that herbivores select food to maximize protein intake (Mattson 1980),while the protein-leverage hypothesis proposes that nutrient intake is governed byprotein-dominated macronutrient balancing (Felton et al. 2009). Because proteinrequirements per unit of body mass tend to increase with decreasing body mass(Lehman 2007), small folivores may be more constrained by low proteinconcentrations in leaves than larger animals.

To circumvent limitations in fiber digestion, folivores have evolved eitherforestomach (colobines, with sacculated stomachs) or ceco-colic, e.g., howlers,indriids, fermentation via symbiotic bacteria hosted in the digestive tract (Chiversand Hladik 1980; Edwards and Ulrey 1999). However, regardless of thesespecializations, primates eat food with highly variable levels of fiber (NationalResearch Council 2003). The absence of a general pattern may be related to the factthat animals with simple stomachs can pass the insoluble fiber quickly through thedigestive system while retaining the cell solubles (van Soest 1996). Fiber toleranceshould be high for midgut fermenters that can retain digestible parts for fermentation(Mackie 2002) and simply expel the indigestible parts through the digestive tractwithout the constraint of rumination (van Soest 1996). In small-bodied fermenters,however, it is still unclear to what extent fiber digestion actually contributes to theenergy supply (Foley and Cork 1992). The positive role of protein and the negativeimpact of fiber have led to the suggestion that the ratio of protein to fiber would limitfolivorous primate populations at least in the Old World (Chapman et al. 2004;Ganzhorn 1992; Oates et al. 1990).

For secondary plant chemicals, the ability of mammalian herbivores to eliminateplant secondary metabolites largely determines which plants they can eat (Marsh etal. 2006; Westoby 1978). Feeding on leaves from a few plant species with specificsecondary substances requires specialized detoxification mechanisms, such as inbamboo lemurs (Hapalemur spp., Prolemur simus), which can detoxify largeamounts of cyanogenic substances from bamboo (Ballhorn et al. 2009; Glander et al.1989; Tan 1999; Yamashita et al. 2010). Generalists should have generalizeddetoxification mechanisms and ingest many different plant species with smallamounts of different secondary substances so that no single secondary chemicalexceeds the threshold at which it might become deleterious (Foley et al. 1999;Freeland and Janzen 1974; Torregrossa et al. 2011).

Primary and secondary metabolites interact. This has been consideredespecially for condensed tannins that can precipitate nutrients and reduce theavailability of nitrogen in food items. The combined effects of primary andsecondary substances can be taken into account either by considering thedifferent components after separate analyses (McKey et al. 1978) or by new formsof analyses that mimic the effect of condensed tannins on protein, but not ofother plant secondary metabolites (DeGabriel et al. 2008; Moore and Foley 2005;Wallis et al. 2011).

152 I. Norscia et al.


Malagasy Folivores

The Malagasy strepsirrhines have adapted to survive long periods of low foodavailability in response to the unpredictable and highly seasonal environment ofMadagascar (Dewar and Richard 2007; Wright 1999). Most of them do not basetheir food choice solely on availability. For example, indriids often use resources thatare underrepresented relative to their consumption (Avahi occidentalis: Thalmann2001; Indri indri: Powzyk and Mowry 2003; Propithecus edwardsi: Hemingway1998; Propithecus verreauxi: Norscia et al. 2006). However, their food selectioncriteria are unclear because they show 1) no preference for leaves with high crudeprotein content (Indri indri, Propithecus diadema, P. coquereli: Ganzhorn 1988;Ganzhorn and Abraham 1991; Powzyk and Mowry 2003; though Avahi laniger. I.indri, and P. coquereli show preferences for high concentrations of soluble protein[Ganzhorn 1988; Ganzhorn and Abraham 1991]); 2) no discrimination against highfiber content (Avahi laniger: Ganzhorn et al. 1985; Indri indri and Propithecusdiadema: Powzyk and Mowry 2003); and 3) either indifference or even a preferencefor condensed tannins (Avahi laniger: Faulkner and Lehman 2006; Ganzhorn 1988;Ganzhorn et al. 1985; Indri indri: Powzyk and Mowry 2003; Propithecus verreauxi:Carrai et al. 2003; Yamashita 2008) or discrimination against tannins (Propithecusverreauxi: Norscia et al. 2006).

Here we explore the feeding patterns of the recently recognized indriid speciesAvahi meridionalis (Southern woolly lemur or fotsife; Zaramody et al. 2006), apair-living lemur, and investigate the relative importance of resource quantity andnutritional quality in influencing their diet. Avahis are particularly intriguing in thiscontext because their body mass is at the lower limits for primate folivores (750–1400 g:Kay 1984; Lehman 2007), they are nocturnal (Norscia and Borgognini-Tarli 2008) andthus active at a time when low ambient temperature possibly increases metabolicrequirements to remain normothermal (Willmer et al. 2000), and their locomotion isenergetically expensive (vertical leaping; Warren and Crompton 1997). Like allindriids, Avahi spp. are anatomical folivores, with a sacculated cecum and a loopedcolon that allow midgut fermentation and no reported detoxification specializations(Chivers and Hladik 1980; Martin 1990). Fermentation in an enlarged cecumoffsets potential limits of the intake of high-fiber food and is important for folivoryin small-bodied mammals (Cork 1996).

We use results from a 7-mo study on Avahi meridionalis as one of the smallestfolivorous primates to address some of the hypotheses described in the precedingtext:

1) Food abundance or dietary choice: Is the diet of Avahi meridionalis defined byfood abundance or food quality?

2) Diet breadth in relation to primary and secondary plant metabolites: Does Avahimeridionalis behave like a generalist or like a specialist? If nutrient constraintsand detoxification limitation apply to Avahi meridionalis, they should include awide array of plant species in their diet.

a) Primary plant chemicals: If the protein maximization hypothesis applies toAvahi meridionalis, their food choice will correlate positively with protein



content. If this species tolerates fiber, fiber content in leaves will notinfluence food selection.

b) Plant secondary metabolites (PSM): If Avahi meridionalis are specialized todetoxify specific PSM, they should tolerate some PSMs but avoid others. IfAvahi meridionalis are generalists, we expect intermediate levels ofingestion of a variety of PSMs.

Methods

Study Site

We conducted this study in the fragment S9 (377 ha) of the pluvial littoral forest ofSainte Luce (southeastern Madagascar: S 24.45′; E 047.11′). This littoral forest ischaracterized by a relatively open and noncontinuous canopy with a height of6–12 m and emergent trees up to 20 m (Bollen and Donati 2005; Gouvenain andSilander 2003). December and January are the wettest and August and September thedriest months, but annual variation in rainfall is high. Between 2000 and 2002 themean annual rainfall was 2690±228 mm (Bollen and Donati 2005; Donati andBorgognini-Tarli 2006). Rainfall from May 2004 to April 2005 was 3850 mm (Fig. 1).Sympatric lemur species at the study site are Avahi meridionalis, Eulemur collaris,Microcebus cf. rufus, Cheirogaleus medius, and Cheirogaleus major.

Focal Species

According to the revision by Zaramody et al. (2006), the species at Sainte Lucerepresents Avahi m. meridionalis that is restricted to the humid forests of southeastMadagascar. Within the littoral forest fragment S9 their density was about 2.6individuals/ha in 2004 (Norscia 2008).

Captures and Observations

In May 2004, Norscia and trained Malagasy assistants darted and radiocollared 4adult Avahi meridionalis (2 males and 2 females belonging to 2 different pairs).Collars consisted of a 22 cm long fabric stripe carrying a 16-g tag that included a TW-3transmitter and a 10- to 28-cell battery with a reduced pulse rate of 43 beats/min. TrainedMalagasy assistants performed the darting during the daytime (on the sleeping trees)with a blowpipe, using pressured narcotic projectiles (Telinject®). We used 4 mg/kgZoletil® 100 for anesthesia (100 mg Tiletamine and Zolazepam 1:1/ml). Both Avahimeridionalis males captured had a body mass of 1100 g. Females had body masses of1250 and 1400 g (both were later found to be pregnant). The groups had home rangesof 2.3–3.5 ha (Norscia and Borgognini-Tarli 2008).

We observed the 4 radiocollared individuals for 7 mo from June to December2004. We recorded the duration of feeding, resting, moving, and other activities, e.g.,grooming, marking, and vocalizations with continuous focal animal sampling(Altmann 1974). We suspended observations when we lost the focal individual. Intotal, we collected 26 nights of observation (total of 256.1 h; 8.5–10.6 h/night). We



marked each tree used by the focal individuals for subsequent identification orsample collection or both.

Vegetation, Food Availability, and Food Quality

From May 2004 to April 2005 we recorded the phenology of 105 treemorphospecies on a monthly basis with the help of a Malagasy assistant (Fig. 1).We classified phenological traits on a 6-level scale (for each item): 000 (absence ofleaves, flowers, or fruits), +00/++0 (progress), +++ (full coverage of leaves, flowers,or fruits), and 0++/00+ (decline) (Norscia et al. 2006). We measured plant speciesabundance by counting the number of trees/morphospecies along a trail 1.5 km longand 10 m wide crossing the S9 fragment, and in 20 squares of 5 m2 in the territory ofthe 2 pairs (thus covering >0.1 ha in total; Keeley and Fotheringham 2005).

We identified the morphospecies of trees in the vegetation plots and thosefrequented by the focal individuals with the help of local botanists. We measured thecircumference at breast height and calculated the diameter at breast height (DBH) ofeach tree included in the territory of Avahi meridionalis. Tree DBH correlates withcrown diameter, making DBH a good indicator of leaf availability (Ganzhorn 2002).

We collected food and nonfood samples for chemical analyses from 1–2 trees perspecies early in the morning (to reduce possible bias related to daily nutrient

Fig. 1 Mean daily rainfall (bars) and phenology of tree morphospecies (% species in each phenologicalphase: lines) from May 2004 to April 2005. Adult leaves were always present in at least 104 out of the 105morphospecies; rainfall data courtesy of Qit Madagascar Minerals.



fluctuations in leaves; Ganzhorn and Wright 1994). We collected food samples(young or adult leaves, flowers) directly from the feeding trees or from trees of thesame species close by. We gathered nonfood samples (only adult leaves) in theterritory of the 2 groups from uneaten plant species. Owing to the difficulty ofdefining nonfood items unambiguously (Janson and Chapman 1999) we countedonly items from plant species that remained uneaten for the entire study period. Weanalyzed air-dried samples, sealed in plastic bags, at the Department of Zoology ofthe University of Hamburg (Germany) for acid detergent fiber (ADF), neutral detergentfiber (NDF), and nitrogen measured via the Kjeldahl method; soluble protein assessedvia Bio-Rad after extraction of the plant material with 0.1 N NaOH for 15 h at roomtemperature; sugar determined as the equivalent of galactose after hydrolizationof 50% methanol extract; condensed tannin (procyanidin tannins) measured asequivalents of quebracho tannin; and polyphenols following Folin-Ciocalteau(Bollen et al. 2004; Stolter et al. 2009). We analyzed alkaloids qualitatively intriple assays for the presence of alkaloids with Mayer’s, Dragendorf’s, andWagner’s reagents (Cromwell 1955). We considered a sample to contain alkaloidsif ≥2 of the reagents showed a positive reaction.

Statistical Analysis

We provide descriptive results for time budget and food item consumption for thecombined samples because the small sample size (N=4 individuals) precludedstatistical analyses at the individual level for the focal individuals. We used Levene’sF and t tests to test for differences within food items and between food and nonfoodsamples with respect to abundance, DBH, and plant chemicals. We arcsinetransformed percentages before analyses. None of the variables deviated fromnormality (Kolmogov-Smirnov test: z<1.05, p>0.05). Feeding time and theproportion of feeding on plant species, families, and food items deviated fromnormality. Therefore we used Spearman rank correlation to investigate therelationship between feeding time and plant species/family abundance and thechemical content of the different food items. We ln transformed proportions offeeding time before fitting a nonlinear regression between feeding time and theconcentrations of polyphenolics in food plants. Significance levels are 2-sided.Analyses follow Siegel and Castellan (1988) and were run with SPSS 12.0 andSTATISTICA 6.0.

Results

The focal individuals became active between 05:34 h and 05:46 h from June toAugust and from 06:05 to 06:46 h between September and December. Duringtheir time of activity, they spent 15% feeding (with a reduction in the middle ofthe night), 67% resting, 14% moving, and 4% in other activities, such as allo-and self-grooming (Fig. 2). They spent 90–100% of their feeding time eatingleaves (Fig. 3).

Avahi meridionalis fed on 125 trees belonging to 43 species and 26 plant families(Table I). The top 2 feeding species, Cynometra cloiselii (Fabaceae) and Plectronia



densiflora (Rubiaceae), accounted for 41% of the total feeding time and the 6 mostpreferred feeding species accounted for about 60% of the total feeding time (Table I).They consumed young leaves and flowers only from September to December, assoon as they became available (Figs. 1 and 3). They limited flower consumptionmostly to green sepals (modified leaves below petals). The subjects never ate fruitseven though they were available throughout the study period (Fig. 1). We found nosignificant difference between the abundance or the DBH of food and nonfood

Fig. 2 Activity budget of Avahi meridionalis at Sainte Luce between 17:00 h and 06:00 h (hatched:resting; gray: feeding; white: moving; black: other).

Fig. 3 Time (%) spent feeding on different food items in June–August and September–December. Theterm “mixed” is used when two items were eaten simultaneously and it was not possible to determine thetime spent feeding on each one.



Table I Plant species, families and % time spent feeding by Avahi meridionalis in Sainte Luce. When thescientific name is not available, we report the Malagasy name

Morphospecies Family Feeding time (%)

Cynometra cloiselii Fabaceae 32.95

Plectronia densiflora Rubiaceae 8.16

Ocotea sp. Lauraceae 5.36

Asteropeia multiflora Asteropeiaceae 4.55

Apodytes sp. Icacinaceae 4.40

Bosqueia sp. Moraceae 4.20

Fandrianakanga 2.59

Intsia bijuga Fabaceae 2.30

Brexia sp. Saxifragaceae 2.25

Nato 2.24

Noronhia sp. Oleaceae 2.13

Tambourissa purpurea Monimiaceae 1.79

Scolopia sp. Flacourtiaceae 1.79

Noronhia cf ovalifolia Oleaceae 1.73

Elaeodendron sp. Celastraceae 1.71

Sarvotaka 1.66

Garcinia sp. Clusiaceae 1.61

Brochoneura acumineata Myristicaceae 1.61

Dracaena reflexa Agavaceae 1.44

Bembicia uniflora Bembiciaceae 1.38

Coffea somersonii Rubiaceae 1.38

Blotia mimosoides Euphorbiaceae 1.33

Sarihapaly 1.33

Varongy 1.09

Tina thouarsiana Sapindaceae 0.86

Cinnamosma madagascariensis Canellaceae 0.86

Dyospiros sp. Ebenaceae 0.81

Rhus thouarsii Anacardiaceae 0.75

Homalium sp. 1 Flacourtiaceae 0.69

Tsarihafotra 0.63

Potameia sp. Lauraceae 0.58

Leptolaena sp. Sarcolaenaceae 0.58

Ludia sp. Flacourtiaceae 0.58

Campylospermum obtusifolium Ochnaceae 0.58

Belschmedia madagascariensis Lauraceae 0.58

Syzigium sp. Myrtaceae 0.58

Homalium albiflorum Flacourtiaceae 0.46

Dycoryphe sp. Hammamelidaceae 0.35

Homalium sp. 2 Flacourtiaceae 0.29

Canarium boivinii Burseraceae 0.23

Rothmannia mandenensis Rubiaceae 0.17

Erythroxylum sp. Liliaceae 0.16

Asteropeia micraster Asteropeiaceae 0.12



tree species (nfood=37, nnonfood=21, abundance: F=0.11, p=0.74; t=1.09, df=56,p=0.28; DBH: F=18.99, p<0.001; t=1.46, df=20.64, p=0.16). The variance ofthe DBH of food trees was lower than that of nonfood trees (mean±standarddeviation: food trees: 8.5±5.2 cm; nonfood trees: 18.5±30.8 cm; F=19.00, p<0.001).There was no significant correlation between the time spent feeding and theabundance of food plant species (n=43, rs=0.10, p=0.55), but a significantpositive correlation between feeding time and the abundance of plant families(rs=0.42, p=0.03, N=26).

In adult leaves, the content of soluble proteins was significantly higher in foodthan in leaves that had not been eaten. Polyphenolics and condensed tannins tendedto have higher concentrations in food than in nonfood leaves, but neither componentdiffered significantly (Table II). The proportion spent feeding on adult leaves fromdifferent species (y; after ln transformation) in relation to the concentrations ofpolyphenolics (x; after arcsine transformation) is best described by a quadraticequation (Fig. 4; ln y=−86.18x2+24.13x −1.20; R2=0.25, F=5.68, p=0.007, df=34).A negative linear regression is also significant but has a lower variance componentexplained by the model (ln y=−9.70x+1.94; R2=0.19, F=8.16, p=0.007, df=35). Noother chemical significantly correlates with feeding time.

As soon as young leaves became available, Avahi meridionalis included youngleaves and flowers in their diet (Fig. 3). Because availability of young leaves andflowers was difficult to quantify and to take into account in the analyses of feedingpreferences, we restrict our analyses of possible preferences by the subjects to simplecomparisons between adult and young leaves. For this comparison, we combinedyoung leaves and flowers. Young leaves contained significantly higher concen-trations of nitrogen and lower concentrations of acid detergent fiber than matureleaves (Table III).

Discussion

Similar to other woolly lemurs (Faulkner and Lehman 2006; Ganzhorn et al. 1985;Harcourt 1991; Thalmann 2001), Avahi meridionalis fed almost exclusively onleaves (Fig. 3), acting as strict folivores. The metabolic constraints associated withthis low-quality diet are exacerbated by expensive locomotion (vertical climbing andleaping; Warren and Crompton 1997, 1998). The constraints of locomotion arereflected in the utilization of trees with trunk diameters that vary little vs. trees notused. This preference of specific supports has also been described for other Avahispecies (Ganzhorn 1989; Warren 1997). Thus, it is not surprising that Avahimeridionalis spent most of the active time resting as a time-minimizing strategyinstead of maximizing energy intake at the expense of long-distance travel (Fig. 2;Hemingway and Bynum 2005). The time-minimizing strategy is associated withdietary choice, modulated by primary and secondary plant metabolites.

Food Abundance or Dietary Choice

As for other indriids (Avahi occidentalis: Thalmann 2001; Indri indri: Powzyk andMowry 2003; Propithecus verreauxi: Norscia et al. 2006), resource abundance was



not the primary criterion for food choice by Avahi meridionalis. There was nodifference between food and nonfood tree species in either abundance or DBH(a proxy for crown size and thus leaf availability). Moreover, we found nocorrelation between the abundance of food plant species in the subjects’ homerange and the time spent feeding on such species. Plant selection independentof availability may be a successful strategy for folivorous lemurs to fulfill theirnutritional demands at fluctuating food availability. The positive correlation

Table II Chemical composition of adult leaves (food and nonfood items) of Avahi meridionalis

Component Food N=37 Nonfood N=20 Statistics

Nitrogen 0.94±0.29 1.06±0.36 t=1.52; p=0.135

Soluble protein 4.58±2.24 3.17±1.73 t=2.34; p=0.023

NDF 43.46±10.21 42.40±10.53 t=0.39; p=0.695

ADF 27.36±6.99 26.75±7.70 t=0.34; p=0.737

Sugar 8.49±9.04 9.04±3.77 t=0.55; p=0.587

Polyphenols 3.91±1.81 3.01±1.60 t=1.96; p=0.055

Condensed tannin 2.28±1.61 1.65±1.49 t=1.73; p=0.091

Alkaloids 52% (N=27) 28% (N=18) χ²=2.57; p=0.109

Values are means ± standard deviations based on the raw data. Percentages were arcsin transformed forstatistical analyses (t-tests for samples with equal variance: F<1.0; p>0.05 for all comparisons). Alkaloidsrepresent the percentage of items with alkaloids. NDF = neutral detergent fibers, ADF = acid detergentfibers

Fig. 4 Linear (R2=0.19) and quadratic regression (R2=0.25) between feeding time and the concentrationof polyphenols in adult leaves consumed by Avahi meridionalis. Concentrations of polyphenolics werearcsine transformed; feeding time was ln transformed.



between the abundance of plant families and the time spent feeding on suchfamilies could be interpreted as a “buffering strategy.” Avahi meridionalis mayswitch to related, nutritionally similar species when their preferred species are notavailable. Staple plant species for other folivorous primates often belong to singleplant families such as Leguminosae, Myrtaceae, or Myristicaceae. This is the casein strepsirrhines, e.g., Lepilemur leucopus (Nash 1998), Avahi occidentalis(Thalmann 2001), Propithecus diadema and Indri indri (Powzyk and Mowry2003), and Propithecus verreauxi (Norscia et al. 2006) and haplorrhines, e.g.,Alouatta pigra (Silver et al. 1998), Colobus polykomos (Dasilva 1994), andPresbytis spp. (Davies et al. 1988).

Diet Breadth: Generalized or Specialized Diets

Influence of Plant Primary Metabolites in Food Choice

Protein content was an important criterion for dietary choice by Avahi meridionalis.The content of soluble proteins was significantly higher in food items than innonfood items and subjects switched to young leaves with higher concentrations ofcrude protein than mature leaves (and identical concentrations of soluble proteins) assoon as young leaves became available (Tables II and III). Leaf selection based on“protein” is a complicated issue. Few studies demonstrated a positive selection forcrude protein, i.e., nitrogen concentration times a conversion factor of 6.25, ascrude protein may not reflect the protein available for digestion because of the

Table III Chemical composition of adult and young leaves and flowers consumed by Avahi meridionalis

Component Adult leaves N=37 Young leaves Statistics

Nitrogen 0.94±0.29 1.90±0.90 (N=10) F=4.71; p=0.035

t=4.08 ; p<0.001

Soluble protein 4.58±2.24 4.71±1.89 (N=11) F=0.21; p=0.647

t=0.32; p=0.749

NDF 43.46±10.21 41.44±10.92 (N=6) F=0.19; p=0.666

t=0.45; p=0.655

ADF 27.36±6.99 19.73±6.01 (N=6) F=0.90; p=0.348

t=2.62; p=0.012

Sugar 8.49±9.04 5.63±3.49 (N=11) F=1.29; p=0.262

t=2.98; p=0.005

Polyphenols 3.91±1.81 4.16±3.40 (N=11) F=3.20; p=0.080

t=0.04; p=0.971

Condensed tannin 2.28±1.61 0.91±1.00 (N=3) F=0.03; p=0.866

t=1.87; p=0.070

Alkaloids 52% (N=27) 60.0% (N=5) χ²=0.24; p=0.626

Values are means ± standard deviations based on the raw data. Percentages were arcsin transformed forstatistical analyses. Alkaloids represent the percentage of items with alkaloids. NDF = neutral detergentfibers; ADF = acid detergent fibers



effects of condensed tannins (Wallis et al. 2011). “Soluble protein” may be anapproximation for “digestible protein” (DeGabriel et al. 2008) and be a morerealistic measure of what is available for digestion than crude protein. InMadagascar, most results showing positive selection for protein by lemurs arebased on soluble proteins and not on crude proteins. In combination, the resultssupport the protein maximization hypothesis.

Food and nonfood items (adult leaves) did not differ significantly in fiber content(Table II). This supports the hypothesis that midgut fermenters do not need todiscriminate strongly against high fiber concentrations (Mackie 2002; van Soest1996). However, Avahi meridionalis included low-fiber food in their diet as soon asit was available. These young leaves and flowers contained significantly lower levelsof acid detergent fiber than adult leaves (Table III). Thus, Avahi meridionalis was notcompletely indifferent to fiber content and therefore the fiber tolerance hypothesisdoes not seem to apply. Although midgut fermentation may allow Avahimeridionalis to partially override the constraints of fiber digestion, cellulose andlignin contained in plant cell walls may still slow down the passage rate of digesta,reduce the amount of food that can be processed per unit time, and reduce nutrientuptake (Campbell et al. 1999, 2000; Mackie 2002; Martin 1990; Milton 1979).Mean gut retention times based on chromium markers (4.5–48.7 h) were found to behighest in folivorous lemurs (Hapalemur griseus and Propithecus verreauxi) andlowest in frugivorous species (Varecia variegata and Eulemur fulvus). Higherretention time increased fiber digestibility (33.1–73.1% for NDF and 7.7–70.6% forADF) (Campbell et al. 2004). Hence, folivores such as Avahi meridionalis need tobalance positive and negative aspects of increased retention time of digesta whenselecting food items.

Influence of Plant Secondary Metabolites in Food Choice

Within the group of plant secondary metabolites, we have to distinguish betweenpossibly toxic substances, such as phenolics and alkaloids and digestion inhibitors,such as condensed tannins. Leaf-eating primates may have buffering mechanisms,such as proline-rich proteins in saliva and a neutral or high pH in the mouth orgut or both, that can reduce the detrimental effects of tannins on proteindigestibility (Ann and Lin 1993; McArthur et al. 1995; Mehansho et al. 1987;Milton 1998; Shimada 2006). Thus, the effect of condensed tannins as digestioninhibitors either could be counterbalanced by specific physiological adaptations, orcondensed tannins may play a role in the context of self-medication, e.g., as anantihemorrhagic or anthelminthic agent (Carrai et al. 2003; Huffman and Chapman2009; Krief et al. 2006; Villalba et al. 2006).

Previous studies suggested that Avahi laniger and A. occidentalis do notdiscriminate against condensed tannins but avoid alkaloids (Ganzhorn 1988). Thishas been interpreted as rather specialized dietary requirements and one of the reasonswhy this species and indriids in general are difficult to keep in captivity. The presentstudy requires refinement of this view. As in the previous study, Avahi meridionalisdid not discriminate against condensed tannins. But they included several plantspecies with alkaloids in their diet. Also, items with intermediate concentrations ofphenolics were eaten most frequently (Fig. 4) and food items contained higher



concentrations of polyphenolics than nonfood items (Table II). Our method for thequantification of polyphenolics measures total phenols, including polyphenolicantioxidants and will react with other reducing substances. These metabolites may betoxic as well as beneficial (Iason 2005). We cannot discriminate between theseoptions with our analysis.

The dietary variation shown by Avahi meridionalis and other folivorous lemurs withno specialized detoxification systems, e.g., Indri indri (Powzyk and Mowry 2003),Propithecus spp. (Irwin 2006), and Lepilemur spp. (Ganzhorn 2002; Thalmann 2001)may allow them to obtain the best mix of nutrients, ensuring toxin dilution (Freelandand Janzen 1974; Westoby 1978; Wiggins et al. 2006). However, 2–6 plant speciesmade up a substantial part of the diet of Avahi meridionalis (40–60%; Table I). Theintermediate level of polyphenolics and the presence of alkaloids in about half of thefood plants classifies Avahi meridionalis as a generalist feeding on many differentplant species with small amounts of different secondary substances so that no singlesecondary chemical exceeds the threshold at which it might become deleterious. Thiscontrasts with the seemingly clear avoidance of alkaloids in previous studies and mayindicate different strategies to deal with possibly toxic substances, i.e., completeavoidance or dilution so as not to exceed a certain threshold concentration.

Conclusions

Our results, along with previous reports, suggest that even generalist folivores needto reach a compromise between strictly specialized and broad folivory. This may bea possible response to nutrient content and the presence of secondary metabolites(Oksanen 1992).

Acknowledgments We thank the Commission Tripartite du Département des Eaux et Forêt, the ParqueBotanique et Zoologique de Tsimbasasa, the Université d’Antananarivo, and Silvana M. Borgognini forresearch permits and support; Qit Madagascar Minerals (QMM) for providing logistic support; the QMMconservation staff: Manon Vincelette for research follow-up and Faly Kandriantafika and DavidRabehevitra for botanical identification of plant species; Givet, Kadoff, Roline, and Josette for theirexcellent help in the field; the people of the villages of Ambandriky and S. Luce for helping in case ofneed. Irene Tomaschewski did a wonderful job for plant analyses. We also thank Elisabetta Palagi and theanonymous reviewers for their thorough and thoughtful suggestions. Joanna Setchell did an outstandingjob providing excellent guidance and editing the manuscript. This research is part of the Ph.D. thesisof I. Norscia partly funded by MIUR.

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