Frugivorous primates are known to encounter many problems to cope with habitat degradation, due to the fluctuating spatial and temporal distribution of their food resources. Since lemur communities evolved strategies to deal with periods of food scarcity, these primates are expected to be naturally adapted to fluctuating ecological conditions and to tolerate a certain degree of habitat changes. However, behavioral and ecological strategies adopted by frugivorous lemurs to survive in secondary habitats have been little investigated. Here, we compared the behavioral ecology of collared lemurs (Eulemur collaris) in a degraded fragment of littoral forest of south-east Madagascar, Mandena, with that of their conspecifics in a more intact habitat, Sainte Luce.
Lemur groups in Mandena and in Sainte Luce were censused in 2004/2007 and in 2000, respectively. Data were collected via instantaneous sampling on five lemur groups totaling 1,698 observation hours. The Shannon index was used to determine dietary diversity and nutritional analyses were conducted to assess food quality. All feeding trees were identified and measured, and ranging areas determined via the minimum convex polygon. In the degraded area lemurs were able to modify several aspects of their feeding strategies by decreasing group size and by increasing feeding time, ranging areas, and number of feeding trees. The above strategies were apparently able to counteract a clear reduction in both food quality and size of feeding trees.
Our findings indicate that collared lemurs in littoral forest fragments modified their behavior to cope with the pressures of fluctuating resource availability. The observed flexibility is likely to be an adaptation to Malagasy rainforests, which are known to undergo periods of fruit scarcity and low productivity. These results should be carefully considered when relocating lemurs or when selecting suitable areas for their conservation.
Citation: Donati G, Kesch K, Ndremifidy K, Schmidt SL, Ramanamanjato J-B, Borgognini-Tarli SM, et al. (2011) Better Few than Hungry: Flexible Feeding Ecology of Collared Lemurs Eulemur collaris in Littoral Forest Fragments. PLoS ONE 6(5): e19807. https://doi.org/10.1371/journal.pone.0019807
Editor: Sharon Gursky-Doyen, Texas A&M University, United States of America
Received: December 26, 2010; Accepted: April 14, 2011; Published: May 19, 2011
Copyright: © 2011 Donati et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The work was funded by Rufford Small Grant for Nature Conservation (http://www.ruffordsmallgrants.org/rsg/Projects/GiuseppeDonati); Qit Madagascar Minerals; Department of Biology, University of Pisa; Department of Anthropology and Geography, Oxford Brookes University; and Department of Animal Ecology and Conservation, University of Hamburg. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
One of the imperative goals of conservation biology is to determine how animals react to habitat degradation and fragmentation. This knowledge is particularly urgent for forest dwelling primates because of the alarming rate of habitat alteration and the scarce ability of most species to move between forest fragments . Habitat loss and fragmentation can alter both quantity and quality of food resources available to primates –. Logging affects density, size, and distribution of plant species in forest fragments , changing the availability of preferred resources for primates, while edge effects result in high mortality of primary forest trees –. However, the primate response to habitat degradation seems to vary depending on species and forest type and no clear generalizations emerge , .
As a general rule, habitat degradation seems to affect to a lesser extent folivorous primates, since secondary growth may produce higher food quality, i.e. leaves with higher protein and lower fiber content, compared with those found in mature forests –. By contrast, frugivorous primates encounter more problems, due to the fluctuating spatial and temporal distribution of fruiting trees, the need to obtain proteins and minerals from alternative food, and larger home range requirements –. Since frugivorous primates are important seed dispersers and therefore fundamental to catalyze the regeneration of degraded habitats, this vulnerability has major implications for the maintenance of forest diversity , . According to evolutionary life history analyses, animals have the option to optimize their energy budget by either minimizing the time spent on food intake (time minimizers) or maximizing the energy intake at the expense of time requirements (energy maximizers) . Different primate species adopt one of the two strategies even though there seem to be some flexibility .
Although Madagascar is experiencing a dramatic habitat loss, how lemurs react to forest degradation and logging is not yet clear , . Similar to other primates, frugivorous lemurs seem to be particularly vulnerable . This disadvantage is amplified by the unpredictability of fruiting patterns which characterizes the island's environment –. Frugivorous ruffed lemurs, Varecia species, for example, are the first to disappear when forest are logged ( but see ). Also, frugivorous rainforest brown lemurs, Eulemur fulvus rufus, are forced to migrate during lean seasons in order to find fruits and meet their energy requirements , . On the other hand, some flexibility has been observed and a number of mainly frugivorous lemurs may switch to lower quality foods during lean periods (E. f. rufus , Lemur catta , V. variegata ), modify their activity and ranging patterns (L. catta , E. macaco flavifrons , E. collaris –), or use food patches of different size and split into subgroups (E. f. fulvus , V. rubra –, V. variegata , Propithecus diadema ). Thus, adaptations to fluctuating ecological conditions may have potentially selected for the ability of lemurs to cope with degraded habitats. However, the question about the limits of tolerance of frugivorous lemurs to secondary and/or degraded habitats and about which strategies they use to deal with these conditions remain unresolved , . Moreover, specific nutritional analyses comparing food items selected in degraded/logged versus intact habitats to assess diet quality have been rarely carried out in Madagascar .
The littoral forest of southern Madagascar offers an excellent opportunity to test the flexibility of frugivorous lemurs to degraded habitats. In 2000 the entire population of collared lemurs, E. collaris, of the Mandena region (MAN) was moved from a forest fragment burned by human activity to a protected, though partially degraded fragment, affected by past logging and edge effect due to its small size . Previously published data indicate that the animals increased body mass on average 15% and their reproductive rate did not differ compared to populations of collared lemurs living in intact habitats. However, the low average group size observed in MAN after the translocation might represent a strategy to reduce feeding competition .
Here, we want to assess whether and how MAN collared lemurs modified their group size, activity budget, diet, and habitat use as a response to habitat degradation. To achieve our goal, we compared the behavioral ecology of MAN groups with data previously collected on lemur groups in the more intact habitat of Ste Luce (STL), a large forest fragment 20 km north of MAN. We predict that:
- MAN lemurs reduce intra-group feeding competition by maintaining a group size smaller than that observed in intact forests.
- MAN lemurs modify their time-budget by increasing feeding and moving effort because of the lower density and quality of food resource in the degraded habitat. Alternatively, resting in MAN lemurs may be increased in order to save energy.
- We also predict that the diet of MAN lemurs is nutritionally poorer and has a higher representation of fall-back species due to the expected lower food availability in the degraded forest.
- Finally, we expect the animals in MAN to modify their habitat use by increasing ranging areas and/or number of feeding trees as a response to increased difficulties in fulfilling nutritional requirements.
Materials and Methods
This study was conducted with the authorization of the Commission Tripartite of the Direction des Eaux et Forêts de Madagascar (Autorisation de recherche #023 MINENVEF/SG/DGEF/DPB/SCBLF/RECH ) and the University of Pisa (Animal Care and Use Board). In accordance with the recommendations of Weatherall report, trapping of the lemurs was conducted entirely under anesthesia using a hypnotic (5 mg/kg of ketamine hydrochloride or tiletamine hydrochloride), so that the animals would not suffer/recall the capture process. Captures were carried out by an experienced Malagasy technician, Enafa Efitroaromy, via a blow-pipe darting. All animals recovered from anesthesia within 1.5 hours and were not moved from the capture area nor kept in a cage, but were followed until regaining full mobility. There were no injuries as a consequence of the captures.
Study Sites and Species
This comparative study was conducted in the littoral forests of MAN and STL near Fort Dauphin in south-eastern Madagascar (Figure 1). Data were first collected in STL in 2000 (fragment S9) and then in MAN in 2004 and 2007 (fragments M15 and M16) (fragment numbering system proceeds from East to West). This region is characterized by a tropical wet climate, with average monthly temperatures of 23°C (range: 18.2–25.9; n = 30), annual rainfall ranging from 1600–2480 mm, and no clear dry season .
Study forest fragments are numbered (modified from ). North is up.
The conservation zone of MAN, 11 km North-West of Fort Dauphin (24°95'S 46°99'E) is located on sandy soils at an altitude 0–20 m above the sea level . The two largest forest fragments in MAN, M15 and M16, cover an area of 148 hectares of degraded littoral forest . Approximately 82 ha of interspersed marsh and swamp connect the two fragments. Because collared lemurs used the swamp for travelling, feeding and resting, we considered these two forest fragments as a single area in this study. M15/M16 are the only two forest fragments where collared lemurs are still present at this site . The average canopy height is 8.9±4.4 m and the understorey is dense . In addition to E. collaris, four nocturnal (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major, Avahi laniger), and one cathemeral lemur species (Hapalemur meridionalis) are found in this area.
The protected forests of STL, around 30 km north of Fort Dauphin (24°45'S 47°11'E), are among the most intact littoral ecosystems in Madagascar and possess a very high vegetation diversity . The 377 ha forest block S9 is one of two fragments where collared lemurs still occur in the STL area . The average canopy height is 14.7±4.3 m with a clearly stratified structure . In addition to E. collaris, four lemur species (Microcebus rufus, Cheirogaleus medius, C. major, Avahi laniger) are found in this area.
Floristically MAN and STL littoral forests are very similar, suggesting that these two areas were once connected . However, structural differences indicate that at the time of study, the forests of MAN represent degraded forms of the vegetation type in STL . This deduction is also suggested by the disappearance of some tree families known to be logged in MAN but not in STL . Forest degradation was evaluated in the two areas by estimating the percentage of surface area occupied by the canopy. This analysis resulted in the two categories of “intact to slightly degraded” and “degraded to highly degraded” for S9 and M15/M16, respectively  .
Phenological records from the region  show that there is a distinct peak in fruit production during the hot-wet season (December-February), while fruit availability is particularly low during the cool-wet season (June-August).
Collared lemurs are arboreal strepsirrhines living in multi-male, multi-female groups . Mean body mass is 2.15±0.25 kg and mean body length is 46.1±2.6 cm (n = 11). Median group size in intact littoral forest is 7 (range: 2–17; n = 13)  and in intact rainforest is 5 (range: 2–7; n = 11) [Johnson, pers. comm.]. This lemur species is cathemeral and its dietary regime is mainly frugivorous .
In order to record group size variations, the total population of E. collaris in MAN was counted by complete censuses in 2004 and 2007. For this exercise, 20 people spaced at 10 m intervals, spanning the width of the M15/M16 forest, walked the entire length of the forest. Surveys usually took one day. In STL, we estimated average group size via line transects . Existing trails that ran in parallel were used as transects when possible to minimize disturbance of the forest. A pair of observers walked four transects (range: 1.5–2.2 km) at a rate of 1 km per hour between the hours of 5am–7am or 4pm–6pm, stopping briefly to scan the forest for indicators of lemur presence. Twelve days per month were spent conducting systematic line transect surveys. A contact time with primate groups of 10 minutes was targeted during line transect censuses.
Diurnal ethological data were collected on five E.collaris groups with different size, 3 in MAN and 2 in STL (Table 1). In MAN data were collected from May to December 2004 and from August to November 2007, while in STL from December 1999 to February 2001. Given the different time window of data collection, to allow comparisons in STL we limited the analyses to the same months when the animals were followed in MAN. Moreover, since nocturnal observations were not possible in MAN, the analysis was limited to the diurnal phase. Overall, 782 observation hours in MAN were compared with 916 hours in STL.
A total of 3 days per month was spent with each group. Each day of observation consisted of 12 consecutive hours of data collection from 6am to 6pm. Individual identification of each study animal was made using nylon collars and colored pendants, and one individual per group was radio-collared. Behavioral data were collected by the instantaneous sampling method with a 5- minute interval . Focal animals were chosen from adult individuals in both study groups, and were rotated every 3 hours, so that all adult group members were evenly sampled at the end of 3 observation days (12 observation hours/day). Instantaneous data collected consisted of animal activity, food type, feeding and resting trees. Activities included feeding (food ingestion), foraging (food exploration), resting, moving, social, and other activities. Food types were noted as fruits, unripe fruits, leaves, young leaves, flowers, invertebrates, and other (bark, stems, roots, mushrooms, decayed wood). Differentiation between unripe/ripe fruits and mature/young leaves was based on differences in color, size, and texture. We estimated lemur diet by using the proportion of feeding records, as the poor visibility conditions in dense littoral forests precluded a reliable quantification of the absolute amount of food items consumed. Although temporal measures of diet may produce significant distortions of actual food intake , , since we focus on the relative proportion of food items between the two forests and not on the absolute quantification of food consumed, this method can be considered adequate for our purposes.
The Shannon index was used to determine the dietary diversity of each population and calculated using the formula: where s is the number of species consumed, pi is the relative abundance of each species in the diet (records spent feeding on species i over the total feeding records). The greater the dietary diversity, the greater is H'. This measure is particularly useful when comparing similar dietary regimes, as it considers both the number of food species and their evenness in the diet.
All feeding trees (i.e. trees where animals were observed feeding at least in one instantaneous record) were marked with a flag and numbered to be found on a subsequent day. After behavioral data were collected, the observer returned to the trees with the help of an assistant to identify the species and to record diameter at breast height (DBH). DBH has been shown to be one of the most accurate proxies to estimate fruit production of trees and has low inter-observer variability . The latitudinal and longitudinal coordinates of the feeding trees were recorded with a GPS and used to determine the size of the ranging area via the minimum convex polygon method performed after having loaded the data in the software RANGES VII.
Biochemical analyses on food items eaten by the two lemur populations were conducted at the Department of Animal Ecology and Conservation of the Hamburg University in 2001 (for STL samples) and 2005–2007 (for MAN samples). Food samples were weighed with an electronic balance (fresh weight), dried in an oven for a standard period, weighed again (dry weight), ground and dried again at 50–60°C before the analyses. The lipid content was determined by extraction using petroleum ether, followed by evaporation of the solvent. Soluble proteins were assessed by BioRad after extraction of the plant material with 0.1 N NaOH for 15 h at room temperature. Soluble carbohydrates and procyanidin (condensed) tannins were extracted with 50% methanol. Concentrations of soluble sugars were determined as the equivalent of galactose after acid hydrolisation of the 50% methanol extract. Samples were analysed for neutral (NDF) and acid (ADF) detergent fibers. NDF represents all the insoluble fiber (cellulose, hemicellulose and lignin), partly digestible in species with hindgut fermentation. ADF represents the fiber fraction containing cellulose and lignin, which are mostly indigestible for Eulemur spp. Polyphenolic concentration was estimated as equivalents to pyrogallic acid units. A detailed review of the procedures and their biological relevance is provided by .
We performed separate nutritional comparisons for fruits and leaves/flowers, due to the expected different contents between these food categories. Additionally, since collared lemurs are mainly frugivorous, in order to focus on potential differences between primary and marginal fruits we compared separately species on which the animals spent at least 1% of their feeding time (primary) and the rest of the sample (marginal). Conversely, since leaves and flowers are used marginally in terms of feeding time, we included in that comparison all items eaten during the study period.
Because of the small sample size and severe deviation from normality, we used the nonparametric Mann-Whitney test to evaluate the differences between median group size recorded at the two sites in 2000, 2004, and 2007. The records of the different activities were weighted by the total number of instantaneous records. Daily average activity frequencies were calculated for each animal during the day. Then, data were pooled by month, and daily grand means per month were obtained at each site. A one-way ANOVA was used to evaluate differences between the two study sites in terms of food nutritional contents. To account for the differences between the two study sites (MAN versus STL), after having controlled for the effect of group size, we used a one-way ANCOVA entering site as independent factor and group size as covariate . For the covariate we used monthly group size after log transformation in order to improve linearity for the regression and then we tested for normality via the Kolmogorov-Smirnov nonparametric test. Units of analysis for the dependent variable were monthly proportions of different activities, monthly proportion of time spent eating different food categories, monthly dietary diversity, monthly ranging areas, monthly average of the daily number of feeding trees, monthly average DBH of feeding trees. Dependent variables were also log-transformed both for the ANOVA and for the ANCOVA. We performed all tests with STATISTICA for Windows, version 6.0 and we considered p<0.05 as the significant level.
Average group size was larger in STL in 2000 (median: 7, range: 2–17, n = 13 groups) than in MAN both in 2004 (median: 3, range: 1–6; n = 11 groups; U = 11, p<0.001) and in 2007 (median: 2, range:1–7; n = 5 groups; U = 7.5, p = 0.010) (Figure 2). Since group composition changed over the study period, data from MAN in 2004 and 2007 were analyzed separately.
Both in STL and in MAN, resting occupied most of the time (±SE: 60.8±1.1%), followed by feeding (14.9±0.8%), moving (13.1±0.1%), social activities (5.6±0.6%), foraging (4.4±2.3%), and other activities (1.2±0.1%) (Figure 3). MAN groups moved significantly more than STL groups (Site effect: F1,21 = 4.566, p = 0.044), once we accounted for the effect of large groups to move more than small groups (Group effect: F1,21 = 12.403, p = 0.002). MAN groups fed significantly more than STL groups (Site effect: F1,21 = 5.014, p = 0.036), once we accounted for the effect of large groups feeding more than small groups (Group effect: F1,21 = 8.293, p = 0.009). Also, STL groups foraged significantly more than MAN groups (Site effect: F1,21 = 12.307, p = 0.002). Though resting and other did not differ between the two sites, small groups rested more and performed in other activities less than large groups (Group effect: F1,21 = 7.601, p = 0.012 for resting; Group effect: F1,21 = 14.892, p<0.001 for other) (Table 2).
Upper quadrant: monthly percentages of instantaneous records. Lower quadrant: residuals of log-transformed time budget controlling for log-transformed group size. Values are means and standard errors. STL: Sainte Luce; MAN: Mandena; * p<.05; ** p<.001.
Collared lemurs were mainly frugivorous (ripe fruits ±SE: 65.7±8.1%; unripe fruits: 4.8±1.1% of total feeding time) at the two sites during the study periods, complementing their diet with flowers (15.7±7.2%), leaves (mature leaves: 5.4±4.5%; young leaves: 4.4±1.5%), invertebrates (4.0±0.8%), and other items (1.2±0.9%) (Figure 4). However, MAN lemurs spent significantly more time eating mature leaves than STL animals (Site effect: F1,21 = 6.690, p = 0.017) (Table 2).
Upper quadrant: monthly percentages of feeding records. Lower quadrant: residuals of log-transformed feeding records controlling for log-transformed group size. Values are means and standard errors. STL: Sainte Luce; MAN: Mandena; * p<.05.
Collared lemurs in STL fed on a total of 75 plant species during the study period while MAN animals used 64 species. Preferred plant species (used for more than 1% of feeding time) accounted for 71% and 89% of feeding time for STL and MAN groups, respectively (Table 3). Monthly dietary diversity evaluated by the Shannon index (H', ±SD: 2.16±0.59 in MAN and 1.78±0.29 in STL) did not differ significantly between sites (Site effect: F1,21 = 2.374, p = 0.138) and there was no influence of group size (group effect: F1,21 = 0.117, p = 0.736).
Nutritional Content of Food
Fruits eaten during more than 1% of feeding time were considered “primary”, those eaten for less than 1% of the time were classified as “marginal”. Due to the small sample size, this distinction was not possible for flowers and leaves.
Nutritional analyses indicate that primary fruits in STL contained a significantly greater proportion of carbohydrates and a lower proportion of lipids as compared to MAN fruits. In contrast, marginal fruits in MAN contained a significantly greater proportion of tannins, fibers, and lipids, and a lower proportion of polyphenolics when compared to STL fruits (Table 4).
As for leaves and flowers consumed, these items in STL contained a significantly greater proportion of carbohydrates and a lower proportion of fibers (both NDF and ADF) than in MAN (Table 4).
MAN groups used monthly ranging areas larger than those used by STL groups (Site effect: F1,21 = 9.606, p = 0.005) after controlling for the effect of large groups to use larger areas (Group effect: F1,21 = 10.201, p = 0.004). Mean monthly ranging areas were (±SD) 28.11±13.28 ha in MAN and 21.15±9.41 ha in STL.
Additionally, MAN lemurs used a significantly higher number of feeding trees per day (Site effect: F1,21 = 10.475, p = 0.004), after controlling for the effect of large groups to use more feeding trees (Group effect: F1,21 = 8.716, p = 0.008). The mean daily number of feeding trees was (±SE) 14.25±3.06 in MAN and 11.91±3.83 in STL.
A total of 734 feeding trees used by the lemur groups in MAN and 1423 in STL were marked and measured. The analysis of the size of feeding trees showed that MAN groups fed on significantly smaller plants, in terms of DBH, as compared to STL groups (Site effect: F1,21 = 6.065, p = 0.023), while group size had no effect on the size of feeding trees (Group effect: F1,21 = 0.076, p = 0.785). The mean monthly DBH of the feeding trees used by the collared lemurs was (±SE) 16.60±3.81 cm in MAN and 21.02±2.78 cm in STL.
In the littoral forest fragments of south-eastern Madagascar collared lemurs exhibited a high degree of social and ecological flexibility. In the degraded area, lemurs were able to modify group size and several aspects of their feeding strategies, by increasing moving and feeding time, ranging areas, and number of feeding trees. Considering that body mass did not differ between the two areas , the above strategies were apparently able to counteract a reduction in both nutritional quality of food items and size of feeding trees in MAN. Our findings are in line with other studies on lemurs that show a relative tolerance to a certain degree of habitat degradation and fragmentation , , , , . However, these results contain relevant implications and potential recommendations for collared lemur conservation in rainforest habitats. First, when living in or moved to degraded habitats these lemurs require much larger ranging areas than in intact or semi-intact forests. Second, in order to counteract intra-group competition they split into small groups with potential effects for demographic dynamics. Though some dietary flexibility has been observed, the above phenomena seem to be the consequence of the incapability of these lemurs to shift to a more folivorous diet, in contrast to what has been observed in other brown lemur populations , .
Our results suggest that the observed reduction in group size in the degraded MAN forest fragment compared to the more intact STL fragment was more likely a consequence of a reduction in habitat size and quality. This response is well known from studies on lemurs and other primates –, , . Predation pressure, the other main factor influencing group size, seems to have represented a less urgent priority for these collared lemurs. In fact, we would expect a larger group size in MAN than in STL, considering that the fossa (Cryptoprocta ferox), the main lemur predator, has not been reported in the latter area in two decades, while it visits MAN occasionally . By the end of 2003 until 2007, some of these carnivores had been seen regularly in the forest. In 2004 only, at least four E. collaris were killed by C. ferox in MAN . The disappearance of several other E. collaris in MAN during the study period may indicate that predation pressure was probably much higher than in STL. Small groups might also have suffered higher predation risk from large diurnal raptors, such as Polyboroides radiatus and Accipiter henstii, both present in the two areas, although attacks were rarely reported .
The increased feeding activity of the MAN lemurs concomitant with greater time spent feeding on leaves or less nutritious food is consistent with patterns observed on other frugivorous-folivorous primates living in fragmented/degraded areas. Howling monkeys (Alouatta palliata) in forest fragments visit more food sources when feeding from more leaves, which results in more traveling and feeding and less resting , , . Low habitat quality is associated with increased feeding and decreased resting in baboons (Theropithecus gelada , Papio cynocephalus ), while an increased feeding on leaves or some fall-back food is also observed in guenons (Cercopithecus cephus ), macaques (Macaca tonkeana ), and lemurs (Propithecus diadema ) living in fragments.
Not surprisingly, the augmented feeding effort recorded in this study seems to have been a direct consequence of spending more time eating mature leaves and low quality food in a habitat impoverished of large fruiting trees. This hypothesis is well supported in our case by the nutritional analyses of all food items, both fruits and leaves/flowers, which showed a drop of carbohydrates and, thus, of available energy for MAN lemurs. Thus, the strategy followed by collared lemurs may have been an increase of feeding efforts in response to a decrease in food energy. This tactic is not a paramount behavioral response, however, and site-specific factors may lead to different choices, even when looking at the same species. Indeed, time-budget differences were not observed in other primates (A. palliata , , Colobus guereza ) when logged and continuous forests are compared. The opposite strategy has also been observed, with decreased feeding and increased resting in other C. guereza groups , in Procolobus rufomitratus , and in Macaca silenus  living in fragmented forests.
Interestingly, another factor possibly accounting for the difference in feeding efforts between MAN and STL may have been the processing time of different food items. We could not collect specific data on processing time, but the top food item in MAN were the drupes of Uapaca ferruginea, which need to be opened to swallow the pulp discarding the husk. Conversely, the top food item in STL were the small berries of Syzigium sp., easily and quickly swallowed without processing. Food processing time is an aspect which deserves further investigation when comparing lemur time-budgets.
Increased feeding on mature leaves, as observed in our lemurs, may also require a greater effort to meet specific nutritional requirements  and to avoid an overload of toxins or digestibility reducing compounds , . This fact would be particularly important for animals with no adaptations for a strictly folivorous diet, such as for Eulemur species . We do not have data on presence/dosage of secondary compounds, tannins and polyphenolics excepted, but an overall tendency for a higher content of the former and a lower content of the latter was observed in MAN food items. These differences were significant in marginal fruits. Tannins, in particular, are known to bind proteins and reduce their digestibility , therefore limiting tannin ingestion might be necessary for MAN lemurs, since their food was extremely poor in proteins (see table 4). The need to limit tannin ingestion may also have restricted the possibility for a more dramatic shift to leaves in our lemurs, since in rainforests leaves are known to contain more secondary compounds and lower protein to fiber ratios, due to their long life-span , . As a matter of fact, Eulemur species in western deciduous forests have been observed to shift to a folivorous diet during some periods of the year , ,  or even year-round , which does not seem to be an option for their congenerics in the eastern rainforests , , . This seems to be the case for our collared lemurs, as the overall time spent feeding on leaves was relatively low in both study areas, though significantly greater in the degraded fragment. Avoiding tannins may be important also when lemurs remain mainly frugivorous, considering the high tannin content and low protein content of the marginal fruits eaten by the MAN lemurs. In support of our findings, a low fruit protein content seems to be a general rule in Madagascar as compared to other continents .
The analysis indicated that, once the effect of group size was removed, collared lemurs in MAN visited more and smaller food trees than those living in the intact forest of STL, which, in turn, resulted in increased ranging areas. This phenomenon may be linked to the fact that MAN groups were not able to feed from large trees, which generally contain more resources and are depleted more slowly . Large trees are in fact the most vulnerable to fragmentation, forest degradation , and human exploitation . The loss of the largest food patches is a general syndrome faced by primates in fragmented forests , , , –, and it might have been the driving force for the observed group size reduction in MAN.
Group fission as a response to changes in food patch size has already been recorded for a number of lemur species –. In this respect, Eulemur species are not an exception . In particular, a 46% decline in average group size of E. f. rufus has been associated with decreased fruit availability in Ranomafana . However, long-term data on this genus from continuous rainforests indicate that habitat shifting is the main response of Eulemur species to severe food scarcity , , . In Ranomafana E. f. rufus are the only lemurs known to migrate up to 5 km away from their home-ranges when fruits are scarce in their habitat . This strategy theoretically allows groups to remain cohesive while they are forced to range further in search for food . Although real migrations have not yet been observed in collared lemurs, the STL largest group was able to expand considerably its monthly ranging area from 23 to 56 ha during the lean season . Such an option was not a choice for the lemurs living in the small MAN fragment, thus possibly forcing animals to split into small subgroups in order to reduce feeding competition. Interestingly, however, groups of lemurs were observed on several occasions to cross the savannah after their translocation into the MAN area, although it is not clear whether this behavior was a response to low food availability or a kind of homing.
Malagasy rainforests are known to naturally experience long periods of fruit scarcity , . Additionally, fruiting tree cycles are irregular  and productivity is relatively low due to poor soils and erratic climate , . This ecological scenario has set the matrix for lemur communities to evolve strategies to deal with periods of food scarcity , . In this respect, frugivorous lemurs are expected to be more resilient to a certain degree of habitat alteration compared to their ecological equivalents in other primate communities , , . Our data indicate that collared lemurs in littoral forest fragments were actually able to modify a number of aspects of their behavioral ecology. However, responses to habitat degradation may change among habitats, species, or even populations , . Additionally, given the potential variation in food availability between years , our conclusions have to be taken with caution until more long-term simultaneous data will be available. Nevertheless, our results contain relevant implications for brown lemur conservation. The observed flexibility in feeding, social, and ranging patterns should be carefully considered when relocating frugivorous lemurs or when selecting suitable areas for their in situ conservation.
This work was carried out under the collaboration agreement between the Department of Animal Biology and Anthropology of the University of Antananarivo, the Institute of Zoology of Hamburg University, and QIT Madagascar Minerals (QMM). We thank the Commission Tripartite of the Malagasy Government, the Ministère des Eaux et Forets, and Missouri Botanical Garden at Antananarivo for their collaboration and permissions to work in Madagascar. We acknowledge Manon Vincelette, Laurent Randrihasipara, Johny Rabenantoandro and Faly Randriatafika of the QMM Environmental Team for providing help at various stages of this research. We are grateful to An Bollen, Nicoletta Baldi, Valentina Morelli for providing additional data on E. collaris feeding ecology from STL. Irene Tomaschewsky helped with plant analyses. Special thanks for the technical assistants of the QMM fauna staff in MAN and STL.
Conceived and designed the experiments: GD JR SMB JUG. Performed the experiments: GD KK KN SLS JR JUG. Analyzed the data: GD KK KN SLS SMB. Contributed reagents/materials/analysis tools: GD JR SMB JUG. Wrote the paper: GD SMB JUG.
- 1. Marsh LK (2003) Primates in fragments: ecology and conservation. New York: Kluwer Academic/Plenum Publishers. 404 p.LK Marsh2003Primates in fragments: ecology and conservation.New YorkKluwer Academic/Plenum Publishers404
- 2. Arroyo-Rodríguez V, Mandujano S (2006) Forest fragmentation modifies habitat quality for Alouatta palliata. Int J Primatol 27: 1079–1096.V. Arroyo-RodríguezS. Mandujano2006Forest fragmentation modifies habitat quality for Alouatta palliata.Int J Primatol2710791096
- 3. Dunn JC, CristóbalAzkarate J, Veà J (2009) Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. Am J Primatol 71: 654–662.JC DunnJ. CristóbalAzkarateJ. Veà2009Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa.Am J Primatol71654662
- 4. Medley KE (1993) Extractive forest resources of the Tana River National Primate Reserve, Kenya. Econ Bot 47: 171–183.KE Medley1993Extractive forest resources of the Tana River National Primate Reserve, Kenya.Econ Bot47171183
- 5. Tutin CEG (1999) Fragmented living: behavioral ecology of primates in a forest fragment in the Lopé reserve, Gabon. Primates 40: 249–265.CEG Tutin1999Fragmented living: behavioral ecology of primates in a forest fragment in the Lopé reserve, Gabon.Primates40249265
- 6. Connor EF, McCoy ED (1974) The statistics and biology of the species-area relationship. Am Nat 113: 791–833.EF ConnorED McCoy1974The statistics and biology of the species-area relationship.Am Nat113791833
- 7. Laurance WF, Delamonica P, Laurance SG, Vasconcelos HL, Lovejoy TE (2000) Rainforest fragmentation kills big trees. Nature 404: 836.WF LauranceP. DelamonicaSG LauranceHL VasconcelosTE Lovejoy2000Rainforest fragmentation kills big trees.Nature404836
- 8. Malcolm JR (1994) Edge effects in central Amazonian forest fragments. Ecology 75: 2438–2445.JR Malcolm1994Edge effects in central Amazonian forest fragments.Ecology7524382445
- 9. Chapman CA, Chapman LJ, Wrangham R, Hunt K, Gebo D, et al. (1992) Estimators of fruit abundance of tropical trees. Biotropica 24: 527–531.CA ChapmanLJ ChapmanR. WranghamK. HuntD. Gebo1992Estimators of fruit abundance of tropical trees.Biotropica24527531
- 10. Cowlishaw G, Dunbar R (2000) Primate conservation biology. Chicago: University of Chicago Press. 498 p.G. CowlishawR. Dunbar2000Primate conservation biology.ChicagoUniversity of Chicago Press498
- 11. Onderdonk DA, Chapman CA (2000) Coping with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21: 587–611.DA OnderdonkCA Chapman2000Coping with forest fragmentation: the primates of Kibale National Park, Uganda.Int J Primatol21587611
- 12. Plumptre AJ, Reynolds V (1994) The effect of selective logging on the primate populations in the Budongo Forest Reserve, Uganda. J Appl Ecol 31: 631–641.AJ PlumptreV. Reynolds1994The effect of selective logging on the primate populations in the Budongo Forest Reserve, Uganda.J Appl Ecol31631641
- 13. Ganzhorn JU (1995) Lowlevel forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology 76: 2084–2096.JU Ganzhorn1995Lowlevel forest disturbance effects on primary production, leaf chemistry, and lemur populations.Ecology7620842096
- 14. Ganzhorn JU, Wright PC, Ratsimbazafy J (1999) Primate communities: Madagascar. In: Fleagle JG, Janson CH, Reed KE, eds. Primate communities. Cambridge: Cambridge University Press. : 75–89.JU GanzhornPC WrightJ. Ratsimbazafy1999Primate communities: Madagascar. In: Fleagle JG, Janson CH, Reed KE, eds. Primate communities.Cambridge: Cambridge UniversityPress. 7589
- 15. Chapman CA, Chapman LJ, Bjorndal K, Onderdonk DA (2002) Application of protein to fiber ratios to predict colobine abundance on different spatial scales. Int J Primatol 23: 283–310.CA ChapmanLJ ChapmanK. BjorndalDA Onderdonk2002Application of protein to fiber ratios to predict colobine abundance on different spatial scales.Int J Primatol23283310
- 16. Estrada A, Coates-Estrada R (1996) Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas. Int J Primatol 5: 759–783.A. EstradaR. Coates-Estrada1996Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas.Int J Primatol5759783
- 17. Lovejoy TE, Bierregaard RO Jr, Rylands AB, Malcom JR, Quintela CE, et al. (1986) Edge and other effects of isolation on Amazon forest fragments. In: Soulé ME, editor. Conservation biology: the science of scarcity and diversity. Sunderland MA: Sinauer Ass. pp. 257–285.TE LovejoyRO Bierregaard JrAB RylandsJR MalcomCE Quintela1986Edge and other effects of isolation on Amazon forest fragments.ME SouléConservation biology: the science of scarcity and diversitySunderland MASinauer Ass257285
- 18. Rode KD, Chapman CA, Mc Dowell LR, Stickler C (2006) Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus ascanius). Biotropica 38: 625–634.KD RodeCA ChapmanLR Mc DowellC. Stickler2006Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus ascanius).Biotropica38625634
- 19. Chapman CA (1995) Primate seed dispersal: co-evolution and conservation implications. Evol Anthrop 4: 74–82.CA Chapman1995Primate seed dispersal: co-evolution and conservation implications.Evol Anthrop47482
- 20. Holloway L (1999) Lemurs can't do it all by themselves anymore. Lemur News 4: 29–30.L. Holloway1999Lemurs can't do it all by themselves anymore.Lemur News42930
- 21. Bollen A, Donati G, Fietz J, Schwab D, Ramanamanjato JB, et al. (2005) An intersite comparison of fruit characteristics in Madagascar: Evidence for selection pressure through abiotic constraints rather than through co-evolution. In: Dew JL, Boubli JP, editors. Tropical fruits and frugivores: The search for strong interactors. Dordrecht: Springer. pp. 93–119.A. BollenG. DonatiJ. FietzD. SchwabJB Ramanamanjato2005An intersite comparison of fruit characteristics in Madagascar: Evidence for selection pressure through abiotic constraints rather than through co-evolution.JL DewJP BoubliTropical fruits and frugivores: The search for strong interactorsDordrechtSpringer93119
- 22. Schoener TW (1971) Theory of foraging strategies. Ann Rev Syst 2: 369–404.TW Schoener1971Theory of foraging strategies.Ann Rev Syst2369404
- 23. Hemingway CA, Bynum N (2005) The influence of seasonality on primate diet and ranging. In: Brockman DK, van Schaik CP, editors. Seasonality in primates: studies of living and extinct human and non-human primates. New York.: Cambridge University Press. pp. 57–104.CA HemingwayN. Bynum2005The influence of seasonality on primate diet and ranging.DK BrockmanCP van SchaikSeasonality in primatesstudies of living and extinct human and non-human primates. New York.: Cambridge University Press57104
- 24. Gardner CJ (2009) A review of the impacts of anthropogenic habitat change on terrestrial biodiversity in Madagascar: implications for the design and management of new protected areas. Malagasy Nature 2: 2–29.CJ Gardner2009A review of the impacts of anthropogenic habitat change on terrestrial biodiversity in Madagascar: implications for the design and management of new protected areas.Malagasy Nature2229
- 25. Irwin MT, Wright PC, Birkinshaw C, Fisher BL, Gardner CJ, et al. (2010) Patterns of species change in anthropogenically disturbed forests of Madagascar. Biol Conserv 143: 2351–2362.MT IrwinPC WrightC. BirkinshawBL FisherCJ Gardner2010Patterns of species change in anthropogenically disturbed forests of Madagascar.Biol Conserv14323512362
- 26. Erhart EM, Overdorff DJ (2008) Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003. Am J Phys Anthrop 136: 183–193.EM ErhartDJ Overdorff2008Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003.Am J Phys Anthrop136183193
- 27. Wright PC (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthrop 42: 31–72.PC Wright1999Lemur traits and Madagascar ecology: coping with an island environment.Yearb Phys Anthrop423172
- 28. Wright PC, Razafindratsita VR, Pochron ST, Jernvall J (2005) The key to Madagascar frugivores. In: Dew JL, Boubli JP, editors. Tropical fruits and frugivores: the search for strong interactors. Dordrecht: Springer. pp. 121–138.PC WrightVR RazafindratsitaST PochronJ. Jernvall2005The key to Madagascar frugivores.JL DewJP BoubliTropical fruits and frugivores: the search for strong interactorsDordrechtSpringer121138
- 29. Dewar RE, Richard AF (2007) Evolution in the hypervariable environment in Madagascar. Proc Natl Acad Sci U S A 104: 13723–13727.RE DewarAF Richard2007Evolution in the hypervariable environment in Madagascar.Proc Natl Acad Sci U S A1041372313727
- 30. White FJ, Overdorff DJ, Balko EA, Wright PC (1995) Distribution of ruffed lemurs (Varecia variegata) in Ranomafana National Park (Madagascar). Folia Primatol 64: 124–131.FJ WhiteDJ OverdorffEA BalkoPC Wright1995Distribution of ruffed lemurs (Varecia variegata) in Ranomafana National Park (Madagascar).Folia Primatol64124131
- 31. Merenlender A , Kremen C , Rakotondratsima M , Weiss A (1998) Monitoring impacts of natural resource extraction on lemurs of the Masoala Peninsula, Madagascar. Conserv Ecol 2: 5.Merenlender AKremen CRakotondratsima MA. Weiss1998Monitoring impacts of natural resource extraction on lemurs of the Masoala Peninsula, Madagascar.Conserv Ecol25
- 32. Overdorff DJ (1993) Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. Int J Primatol 14: 721–753.DJ Overdorff1993Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar.Int J Primatol14721753
- 33. Sussman RW (1974) Ecological distinctions in sympatric species of Lemurs. In: Martin RD, Doyle GA, Walker AC, editors. Prosimian biology. London: Duckworth. pp. 75–108.RW Sussman1974Ecological distinctions in sympatric species of Lemurs.RD MartinGA DoyleAC WalkerProsimian biologyLondonDuckworth75108
- 34. Gould L, Sussman RW, Sauther ML (1999) Natural disasters and primate populations: the effects of a 2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in Southwestern Madagascar. Int J Primatol 20: 69–84.L. GouldRW SussmanML Sauther1999Natural disasters and primate populations: the effects of a 2-year drought on a naturally occurring population of ring-tailed lemurs (Lemur catta) in Southwestern Madagascar.Int J Primatol206984
- 35. Ratsimbazafy JH, Ramarosandratana HV, Zaonarivelo RJ (2002) How do black-and-white ruffed lemurs still survive in a highly disturbed habitat? Lemur News 7: 7–10.JH RatsimbazafyHV RamarosandratanaRJ Zaonarivelo2002How do black-and-white ruffed lemurs still survive in a highly disturbed habitat?Lemur News7710
- 36. Pereira ME, Strohecker RA, Cavigelli SA, Hughes CL, Pearson DD (1999) Metabolic strategy and social behavior in Lemuridae. In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM, editors. New directions in lemur studies. New York: Kluwer. pp. 93–118.ME PereiraRA StroheckerSA CavigelliCL HughesDD Pearson1999Metabolic strategy and social behavior in Lemuridae.B. RakotosamimananaH. RasamimananaJU GanzhornSM GoodmanNew directions in lemur studiesNew YorkKluwer93118
- 37. Schwitzer N, Kaumanns W, Seitz IC, Schwitzer C (2007) Cathemeral activity patterns of the blue-eyed black lemur (Eulemur macaco flavifrons) in intact and degrader forest fragments. End Species Res 3: 239–247.N. SchwitzerW. KaumannsIC SeitzC. Schwitzer2007Cathemeral activity patterns of the blue-eyed black lemur (Eulemur macaco flavifrons) in intact and degrader forest fragments.End Species Res3239247
- 38. Donati G, Bollen A, Borgognini-Tarli SM, Ganzhorn JU (2007a) Feeding over the 24-hour cycle: dietary flexibility of cathemeral collared lemurs (Eulemur collaris). Behav Ecol Sociobiol 61: 1237–1251.G. DonatiA. BollenSM Borgognini-TarliJU Ganzhorn2007aFeeding over the 24-hour cycle: dietary flexibility of cathemeral collared lemurs (Eulemur collaris).Behav Ecol Sociobiol6112371251
- 39. Donati G, Baldi N, Morelli V, Ganzhorn JU, Borgognini-Tarli SM (2009) Proximate cues and ultimate determinants of brown lemur cathemerality. An Behav 77: 317–325.G. DonatiN. BaldiV. MorelliJU GanzhornSM Borgognini-Tarli2009Proximate cues and ultimate determinants of brown lemur cathemerality.An Behav77317325
- 40. Ganzhorn JU (1988) Food partitioning among Malagasy primates. Oecologia 75: 436–450.JU Ganzhorn1988Food partitioning among Malagasy primates.Oecologia75436450
- 41. Vasey N (1997) The social behavior of red-ruffed lemurs (Varecia variegata rubra) in Masoala peninsula. PhD Thesis, Washington University, St. Louis Missouri. N. Vasey1997The social behavior of red-ruffed lemurs (Varecia variegata rubra) in Masoala peninsula.PhD Thesis, Washington University, St. Louis Missouri
- 42. Vasey N (2003) Varecia, ruffed lemurs. In: Goodman SM, Benstead JP, editors. The natural history of Madagascar. New York: Aldine de Gruyter. pp. 1332–1336.N. Vasey2003Varecia, ruffed lemurs.SM GoodmanJP BensteadThe natural history of MadagascarNew YorkAldine de Gruyter13321336
- 43. Balko EA (1998) The behavioral plasticity of Varecia variegata in Ranomafana National Park, Madagascar. PhD Thesis, SUNY-College of Environmental Science and Forestry, Syracuse, NY. EA Balko1998The behavioral plasticity of Varecia variegata in Ranomafana National Park, Madagascar.PhD Thesis, SUNY-College of Environmental Science and Forestry, Syracuse, NY
- 44. Irwin MT (2007) Living in forest fragments reduces group cohesion in diademed Sifakas (Propithecus diadema) in Eastern Madagascar by reducing food patch size. Am J Primatol 69: 434–447.MT Irwin2007Living in forest fragments reduces group cohesion in diademed Sifakas (Propithecus diadema) in Eastern Madagascar by reducing food patch size.Am J Primatol69434447
- 45. Lehman SM, Rajaonson A, Day S (2006) Edge effects and their influence on lemur density and distribution in southeast Madagascar. Am J Phys Anthrop. 129. : 232–241.SM LehmanA. RajaonsonS. Day2006Edge effects and their influence on lemur density and distribution in southeast Madagascar.Am J Phys Anthrop129232241
- 46. Rabenantoandro J, Randriatafika F, Lowry IIPP (2007) Floristic and structural characteristics of remnant littoral forest sites in the Tolagnaro area. In: Ganzhorn JU, Goodman SM, Vincelette M, editors. Biodiversity, ecology and conservation of the littoral ecosystems of South-eastern Madagascar. Washington DC: Smithsonian Institution Press. pp. 65–77.J. RabenantoandroF. RandriatafikaIIPP Lowry2007Floristic and structural characteristics of remnant littoral forest sites in the Tolagnaro area.JU GanzhornSM GoodmanM. VinceletteBiodiversity, ecology and conservation of the littoral ecosystems of South-eastern MadagascarWashington DCSmithsonian Institution Press6577
- 47. Donati G, Ramanamanjato JB, Ravoahangy AM, Vincelette M (2007b) Translocation as a conservation measure for a threatened species: the case of Eulemur collaris in the Mandena littoral forest, south-eastern Madagascar. In: Ganzhorn JU, Goodman SM, Vincelette M, editors. Biodiversity, ecology and conservation of the littoral ecosystems of South-eastern Madagascar. Washington DC: Smithsonian Institution Press. pp. 237–243.G. DonatiJB RamanamanjatoAM RavoahangyM. Vincelette2007bTranslocation as a conservation measure for a threatened species: the case of Eulemur collaris in the Mandena littoral forest, south-eastern Madagascar.JU GanzhornSM GoodmanM. VinceletteBiodiversity, ecology and conservation of the littoral ecosystems of South-eastern MadagascarWashington DCSmithsonian Institution Press237243
- 48. Bollen , A , Donati G (2005) Phenology of the littoral forest of Sainte Luce, Southeastern Madagascar. Biotropica, 37: 32–43.BollenAG. Donati2005Phenology of the littoral forest of Sainte Luce, Southeastern Madagascar.Biotropica,373243
- 49. Vincelette M, Theberge M, Randrihasipara L (2007) Evaluations of forest cover at regional and local levels in the Tolagnaro region since 1950. In: Ganzhorn JU, Goodman SM, Vincelette M, editors. Biodiversity, ecology and conservation of the littoral ecosystems of South-eastern Madagascar. Washington DC: Smithsonian Institution Press. pp. 49–58.M. VinceletteM. ThebergeL. Randrihasipara2007Evaluations of forest cover at regional and local levels in the Tolagnaro region since 1950.JU GanzhornSM GoodmanM. VinceletteBiodiversity, ecology and conservation of the littoral ecosystems of South-eastern MadagascarWashington DCSmithsonian Institution Press4958
- 50. Ganzhorn JU, Andrianasolo T, Andrianjazalahatra T, Donati G, Fietz J, et al. (2007) Lemurs in evergreen littoral forest fragments of different size and degrees of degradation. In: Ganzhorn JU, Goodman SM, Vincelette M, editors. Biodiversity, ecology and conservation of the littoral ecosystems of South-eastern Madagascar. Washington DC: Smithsonian Institution Press. pp. 223–236.JU GanzhornT. AndrianasoloT. AndrianjazalahatraG. DonatiJ. Fietz2007Lemurs in evergreen littoral forest fragments of different size and degrees of degradation.JU GanzhornSM GoodmanM. VinceletteBiodiversity, ecology and conservation of the littoral ecosystems of South-eastern MadagascarWashington DCSmithsonian Institution Press223236
- 51. Bollen A, Donati G (2006) Conservation status of the littoral forest of south-eastern Madagascar: a review. Oryx 40: 57–66.A. BollenG. Donati2006Conservation status of the littoral forest of south-eastern Madagascar: a review.Oryx405766
- 52. Ross C, Reeve N (2003) Survey and census methods: population density and distribution. In: Setchell JM, Curtis DJ, editors. Field and laboratory methods in Primatology: A practical guide. New York: Cambridge University Press. pp. 90–109.C. RossN. Reeve2003Survey and census methods: population density and distribution.JM SetchellDJ CurtisField and laboratory methods in Primatology: A practical guideNew YorkCambridge University Press90109
- 53. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49: 227–267.J. Altmann1974Observational study of behaviour: sampling methods.Behaviour49227267
- 54. Kurland JA, Gaulin SJC (1987) Comparability among measures of primate diets. Primates 28: 71–77.JA KurlandSJC Gaulin1987Comparability among measures of primate diets.Primates287177
- 55. Zinner D (1999) Relationship between feeding time and food intake in hamadryas baboons (Papio hamadryas) and the value of feeding time as predictor of food intake. Zoo Biol 18: 495–505.D. Zinner1999Relationship between feeding time and food intake in hamadryas baboons (Papio hamadryas) and the value of feeding time as predictor of food intake.Zoo Biol18495505
- 56. Ortmann S, Bradley BJ, Stolter C, Ganzhorn JU (2006) Estimating the quality and composition of wild animal diets-a critical survey of methods. In: Hohmann G, Robbins MM, Boesch C, editors. Feeding ecology in apes and other primates. Ecological, physical and behavioural aspects. Cambridge: Cambridge University Press. pp. 397–420.S. OrtmannBJ BradleyC. StolterJU Ganzhorn2006Estimating the quality and composition of wild animal diets-a critical survey of methods.G. HohmannMM RobbinsC. BoeschFeeding ecology in apes and other primates. Ecological, physical and behavioural aspectsCambridgeCambridge University Press397420
- 57. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge: Cambridge University Press. 537 p.GP QuinnMJ Keough2002Experimental design and data analysis for biologists.CambridgeCambridge University Press537
- 58. Rasmussen MA (1999) Ecological influences on activity cycle in two cathemeral primates, Eulemur mongoz (mongoose lemur) and Eulemur fulvus fulvus (common brown lemur). PhD Thesis, Duke University, Durham, North Carolina. MA Rasmussen1999Ecological influences on activity cycle in two cathemeral primates, Eulemur mongoz (mongoose lemur) and Eulemur fulvus fulvus (common brown lemur).PhD Thesis, Duke University, Durham, North Carolina
- 59. Van Hooff JARAM, Van Schaik CP (1992) Cooperation in competition: The ecology of primate bonds. In: Harcourt AH, de Waal FBM, editors. Coalitions and alliances in humans and other animals. Oxford: Oxford Science Publications. pp. 357–389.JARAM Van HooffCP Van Schaik1992Cooperation in competition: The ecology of primate bonds.AH HarcourtFBM de WaalCoalitions and alliances in humans and other animalsOxfordOxford Science Publications357389
- 60. Barton RA, Byrne R, Whiten A (1996) Ecology, feeding competition and social structure in baboons. Behav Ecol Sociobiol 38: 321–329.RA BartonR. ByrneA. Whiten1996Ecology, feeding competition and social structure in baboons.Behav Ecol Sociobiol38321329
- 61. Clarke MR, Collins AD, Zucker EL (2002) Responses to deforestation in a group of mantled howlers (Alouatta palliata) in Costa Rica. Int J Primatol 23: 365–381.MR ClarkeAD CollinsEL Zucker2002Responses to deforestation in a group of mantled howlers (Alouatta palliata) in Costa Rica.Int J Primatol23365381
- 62. Dunn JC, Cristóbal-Azkarate J, Veà JJ (2010) Seasonal variations in the diet and feeding effort of two groups of howlers in different sized forest fragments. Int J Primatol 31: 887–903.JC DunnJ. Cristóbal-AzkarateJJ Veà2010Seasonal variations in the diet and feeding effort of two groups of howlers in different sized forest fragments.Int J Primatol31887903
- 63. Iwamoto T, Dunbar RIM (1983) Thermoregulation, habitat quality, and the behavioral ecology of gelada baboons. J An Ecol 52: 357–366.T. IwamotoRIM Dunbar1983Thermoregulation, habitat quality, and the behavioral ecology of gelada baboons.J An Ecol52357366
- 64. Altmann J, Muruthi P (1988) Differences in daily life between semi-provisioned and wild-feeding baboons. Am J Primatol 15: 213–221.J. AltmannP. Muruthi1988Differences in daily life between semi-provisioned and wild-feeding baboons.Am J Primatol15213221
- 65. Riley EP (2007) Flexibility in diet and activity patterns of Macaca tonkeana in response to anthropogenic habitat alteration. Int J Primatol 28: 107–133.EP Riley2007Flexibility in diet and activity patterns of Macaca tonkeana in response to anthropogenic habitat alteration.Int J Primatol28107133
- 66. Irwin MT (2008) Feeding ecology of Propithecus diadema in forest fragments and continuous forest. Int J Primatol 29: 95–115.MT Irwin2008Feeding ecology of Propithecus diadema in forest fragments and continuous forest.Int J Primatol2995115
- 67. Bicca-Marques JC (2003) How do howler monkeys cope with habitat fragmentation? In: Marsh LK, editor. Primates in fragments: ecology and conservation. New York: Kluwer Academic/Plenum Press. pp. 283–303.JC Bicca-Marques2003How do howler monkeys cope with habitat fragmentation?LK MarshPrimates in fragments: ecology and conservationNew YorkKluwer Academic/Plenum Press283303
- 68. Cristóbal-Azkarate J, Arroyo-Rodríguez V (2007) Diet and activity patterns of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation. Am J Primatol 69: 1–17.J. Cristóbal-AzkarateV. Arroyo-Rodríguez2007Diet and activity patterns of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation.Am J Primatol69117
- 69. Oates JF (1977) The guereza and its food. In: Clutton-Brock TH, editor. Primate ecology: Studies of feeding and ranging behavior in lemurs, monkeys, and apes. London: Academic Press. pp. 276–321.JF Oates1977The guereza and its food.TH Clutton-BrockPrimate ecology: Studies of feeding and ranging behavior in lemurs, monkeys, and apesLondonAcademic Press276321
- 70. Marsh CW (1981) Time budget of Tana river red colobus. Folia Primatol 35: 30–50.CW Marsh1981Time budget of Tana river red colobus.Folia Primatol353050
- 71. Menon S, Poirier FE (1996) Lion-tailed macaques (Macaca silenus) in a disturbed forest fragment: Activity patterns and time budget. Int J Primatol 17: 969–985.S. MenonFE Poirier1996Lion-tailed macaques (Macaca silenus) in a disturbed forest fragment: Activity patterns and time budget.Int J Primatol17969985
- 72. Nagy KA, Milton K (1979) Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata). Ecology 60: 475–480.KA NagyK. Milton1979Energy metabolism and food consumption by wild howler monkeys (Alouatta palliata).Ecology60475480
- 73. Freeland WJ, Janzen DH (1974) Strategies of herbivory in mammals: the role of plant secondary compounds. Am Nat 108: 269–289.WJ FreelandDH Janzen1974Strategies of herbivory in mammals: the role of plant secondary compounds.Am Nat108269289
- 74. Glander KE (1981) Feeding patterns in mantled howling monkeys. In: Kamil AC, Sargent TD, editors. Foraging behavior: Ecological, ethological, and psychological approaches. New York: Garland Press. pp. 231–255.KE Glander1981Feeding patterns in mantled howling monkeys.AC KamilTD SargentForaging behavior: Ecological, ethological, and psychological approachesNew YorkGarland Press231255
- 75. Overdorff DJ, Rasmussen MA (1995) Determinants of nighttime activity in “diurnal” lemurid primates. In: Alterman LG, Doyle GA, Izard K, editors. Creatures of the dark: The nocturnal prosimians. New York: Plenum. pp. 1–74.DJ OverdorffMA Rasmussen1995Determinants of nighttime activity in “diurnal” lemurid primates.LG AltermanGA DoyleK. IzardCreatures of the dark: The nocturnal prosimiansNew YorkPlenum174
- 76. DeGabriel JL, Moore BD, Foley WJ, Johnson CN (2009) The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90: 711–719.JL DeGabrielBD MooreWJ FoleyCN Johnson2009The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal.Ecology90711719
- 77. Coley PD (1983) Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecol Mon 53: 209–233.PD Coley1983Herbivory and defensive characteristics of tree species in a lowland tropical forest.Ecol Mon53209233
- 78. Reich PB (2001) Body size, geometry, longevity and metabolism: do plant leaves behave like animal bodies? Trends Ecol Evol 16: 674–680.PB Reich2001Body size, geometry, longevity and metabolism: do plant leaves behave like animal bodies?Trends Ecol Evol16674680
- 79. Curtis DJ, Zaramody A, Martin RD (1999) Cathemeral activity in the mongoose lemur, Eulemur mongoz. Am J Primatol 47: 279–298.DJ CurtisA. ZaramodyRD Martin1999Cathemeral activity in the mongoose lemur, Eulemur mongoz.Am J Primatol47279298
- 80. Donati G, Lunardini A, Kappeler PM (1999) Cathemeral activity of red-fronted brown lemurs (Eulemur fulvus rufus) in the Kirindy Forest/CFPF. In: Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM, editors. New directions in lemur studies. New York: Plenum. pp. 119–137.G. DonatiA. LunardiniPM Kappeler1999Cathemeral activity of red-fronted brown lemurs (Eulemur fulvus rufus) in the Kirindy Forest/CFPF.B. RakotosamimananaH. RasamimananaJU GanzhornSM GoodmanNew directions in lemur studiesNew YorkPlenum119137
- 81. Ganzhorn JU, Arrigo-Nelson S, Bollen A, Carrai V, Chalise MK, et al. (2009) Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PLoS One 4(12): e8253.JU GanzhornS. Arrigo-NelsonA. BollenV. CarraiMK Chalise2009Possible fruit protein effects on primate communities in Madagascar and the Neotropics.PLoS One412e8253
- 82. Leighton M, Leighton DR (1982) The relationship of size of feeding aggregate to size of food patch: Howler monkeys (Alouatta palliata) feeding in Trichilia cipo fruit trees on Barro Colorado Island. Biotropica 14: 81–90.M. LeightonDR Leighton1982The relationship of size of feeding aggregate to size of food patch: Howler monkeys (Alouatta palliata) feeding in Trichilia cipo fruit trees on Barro Colorado Island.Biotropica148190
- 83. Strier K (1989) Effects of patch size on feeding associations in Muriquis (Brachyteles arachnoides). Folia Primatol 52: 70–77.K. Strier1989Effects of patch size on feeding associations in Muriquis (Brachyteles arachnoides).Folia Primatol527077
- 84. Stevenson PR, Quinones MG, Ahumada JA (1998) Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species at Tinigua National Park, Colombia. Int J Primatol 19: 313–324.PR StevensonMG QuinonesJA Ahumada1998Effects of fruit patch availability on feeding subgroup size and spacing patterns in four primate species at Tinigua National Park, Colombia.Int J Primatol19313324
- 85. Overdorff DJ, Merenlender AM, Talata P, Telo A, Forward ZA (1999) Life history of Eulemur fulvus rufus from 1988–1998 in southeastern Madagascar. Am J Phys Anthrop 108: 295–310.DJ OverdorffAM MerenlenderP. TalataA. TeloZA Forward1999Life history of Eulemur fulvus rufus from 1988–1998 in southeastern Madagascar.Am J Phys Anthrop108295310
- 86. Donati G (2002) The activity cycle and its ecological correlates in the collared brown lemur, Eulemur fulvus collaris (Lemuridae), in the littoral forest of Ste Luce (Fort Dauphin, Madagascar). PhD thesis, University of Pisa. G. Donati2002The activity cycle and its ecological correlates in the collared brown lemur, Eulemur fulvus collaris (Lemuridae), in the littoral forest of Ste Luce (Fort Dauphin, Madagascar).PhD thesis, University of Pisa
- 87. Richard AF, Dewar RE (1991) Lemur ecology. Ann Rev Ecol Syst 22: 145–175.AF RichardRE Dewar1991Lemur ecology.Ann Rev Ecol Syst22145175