International Journal of Primatology

, Volume 32, Issue 3, pp 566–586 | Cite as

Seasonal Changes in Feeding Ecology and Activity Patterns of Two Sympatric Mouse Lemur Species, the Gray Mouse Lemur (Microcebus murinus) and the Golden-brown Mouse Lemur (M. ravelobensis), in Northwestern Madagascar

  • Sandra Thorén
  • Franziska Quietzsch
  • Doreen Schwochow
  • Lalandy Sehen
  • Christopher Meusel
  • Kate Meares
  • Ute Radespiel
Article

Abstract

Because closely related species are likely to be ecologically similar owing to common ancestry, they should show some degree of differentiation in order to coexist. We studied 2 morphologically similar congeneric species, the golden-brown mouse lemur (Microcebus ravelobensis) and the gray mouse lemur (M. murinus). These species are found in partial sympatry in the dry deciduous forest in northwestern Madagascar. We investigated whether 1) feeding niche differentiation and/or 2) a reduction in locomotor activity during periods of food shortage, which might reflect an energy saving strategy, can explain the coexistence of these 2 lemur species. To obtain feeding and behavioral data, we conducted focal observations of 11 female Microcebus murinus and 9 female M. ravelobensis during 11 months from 2007 to 2008 and collected fecal samples for 6 mo. We monitored the phenology of 272 plant specimens and trapped arthropods to determine food availability. Results revealed interspecific differences in 1) relative proportion of consumed food resources, resulting in a merely partial dietary overlap, and in 2) relative importance of seasonally varying food resources throughout the year. In addition, females of Microcebus murinus showed a reduction in locomotor activity during the early dry season, which might reflect an energy-saving strategy and might further reduce potential competition with M. ravelobensis over limited food resources. To conclude, a combination of interspecific feeding niche differentiation and differences in locomotor activity appears to facilitate the coexistence of Microcebus murinus and M. ravelobensis.

Keywords

Activity budget Diet Feeding ecology Niche differentiation Seasonality 

Introduction

Stable coexistence of species in homogeneous and saturated environments requires that species possess ecologically different niches to avoid or reduce interspecific competition for essential resources (Amarasekare 2003; Brown and Wilson 1956; Chase and Leibold 2003; Gause 1934; Hardin 1960). As observed in numerous sympatric species (arthropods: Behmer and Joern 2008; invertebrates: Pianka 1973; birds: Garcia and Arroyo 2005, mammals: Azevedo et al.2006; Sushma and Singh 2006), feeding niche differentiation may enable coexistence of species. In primates, feeding niche differentiation may be expressed as 1) food partitioning (Ganzhorn 1988, 1989; Houle et al.2006; Peres 1993; Thalmann 2001), 2) temporal partitioning of food resources (Bearder and Doyle 1974; Cox and Moore 2000; Petter 1962), and 3) spatial partitioning of food resources (Dammhahn and Kappeler 2008a; Ganzhorn 1989; Lahann 2007, 2008; Rakotondravony and Radespiel 2009; Rendigs et al.2003; Schwab and Ganzhorn 2004). Food partitioning includes many different aspects of dietary differences. For instance, species might choose food items with different chemical properties, which was suggested to separate coexisting lemur species ecologically in the eastern rain forest of Madagascar (Ganzhorn 1989). In other cases, dietary differences are more pronounced. For instance, Thalmann (2001) found clear dietary differences between 2 folivorous species of similar size, Lepilemur edwardsi and Avahi occidentals. These differences were in fact even more pronounced when taking seasonality into account. Temporal separation of resource use can also be expressed on a daily basis as diurnal versus nocturnal feeding pattern (Petter 1962). Species can also differ in how they exploit resources. In Uganda, the frugivorous species Cercopithecus mitis and C. ascanius differ in how much food they generally leave behind in a food patch, indicating a difference in feeding efficiency at low fruit densities. Their coexistence seems to be enabled by Cercopithecus ascanius being able to survive on low fruits densities while the dominant C. mitis is able to aggressively defend resources. Sometimes differences in feeding ecology fail to explain the coexistence of species, but it seems instead to be facilitated by a spatial separation of species like in the case of Microcebus murinus and M. berthae in western Madagascar (Dammhahn and Kappeler 2008a, b) and Cheirogaleus medius, C. major, and Microcebus murinus in southeastern Madagascar (Lahann 2007, 2008).

Differentiated feeding niches of coexisting species should be especially important during periods of food shortage to avoid competition over limited food resources (Hladik et al.1980). Alternatively, competition over food resources can be reduced if competing species can minimize their energetic requirements. For instance, many Cheirogaleids enter daily torpor (Microcebus spp.: Schmid 1999, 2000; Schmid and Ganzhorn 2009) or hibernate (Microcebus spp.: Atsalis 1999; Schmid and Ganzhorn 2009; Cheirogaleus medius: Dausmann et al.2004, 2005; C. major: Fietz and Ganzhorn 1999) during periods of low ambient temperatures and food shortage. These physiological strategies reduce energetic costs to varying extents (Kobbe and Dausmann 2009; Schmid and Kappeler 2005; Schmid et al.2000; Schülke and Ostner 2007) and might reduce competition over limited food resources and therefore facilitate coexistence of species. For instance, in western Madagascar, Cheirogaleus medius possess the ability to hibernate for up to 7 mo a year during the dry season, which might help to explain its coexistence with the much smaller Microcebus berthae (Dausmann et al.2005).

More than 90 species of endemic primates occur in Madagascar (Mittermeier et al.2008), all belonging to the order Lemuriformes, with up to 14 species coexisting in a single forest (Ganzhorn et al.1999; Rasolofoson et al.2007). The extraordinary high local diversity of lemur species, and the fact that the majority of these species are locally restricted, make lemurs particularly interesting for the study of species coexistence. We studied the sympatric congeneric lemur species the gray mouse lemur (Microcebus murinus) and the golden-brown mouse lemur (M. ravelobensis), that are found in partial sympatry in northwestern Madagascar. Microcebus murinus inhabits a wide range of habitats from the south to the northwest of the island, and is found in sympatry with 2 other well studied congeneric species in other areas (M. berthae in western Madagascar: Dammhahn and Kappeler 2005; 2008a; Schwab 2000; Schwab and Ganzhorn 2004; M. griseorufus in southwestern Madagascar: Génin 2008; Rasoazanabary 2004; Yoder et al.2002). Microcebus ravelobensis, on the other hand, is limited to the dry deciduous forests located in the area between 2 large rivers, the Betsiboka and the Mahajamba (Olivieri et al.2007; Rakotondravony and Radespiel 2009). Microcebus murinus and M. ravelobensis occur in zones of extensive spatial overlap, with a confirmed coexistence of ≥15 yr in certain forest patches (Mester 2006; Rendigs et al.2003; Zimmermann et al.1998), where they potentially compete over limited food resources, particularly in the lean dry period (Rakotondravony and Radespiel 2009; Zimmermann et al.1998).

Microcebus murinus and M. ravelobensis are very similar morphologically. They do not differ in body length (Microcebus murinus: 83.3 ± 0.9 mm, M. ravelobensis: 81.3 ± 1.9 g) or body mass (M. murinus: 53.9 ± 0.9 g, M. ravelobensis: 56.2 ± 1.8 g; Zimmermann et al.1998). However, Microcebus murinus has a thicker and longer tail than M. ravelobensis does (M. murinus: 24.5 ± 0.5 mm, 128.4 ± 1.1 mm; M. ravelobensis: 18.2 ± 0.8 mm, 157.1 ± 2.5 mm; Zimmermann et al.1998). Both species feed on gum, insect secretions, nectar, fruits, and animal matter (Joly and Zimmermann 2007; Radespiel et al.2006). A preliminary study suggests that they differ in diet composition. However, the study was carried out during a restricted period, and did not take seasonally dietary changes into account (Radespiel et al.2006).

In northwestern Madagascar, Microcebus ravelobensis as well as M. murinus have been observed only to enter daily torpor (inferred from trapping data and sleeping site controls: Radespiel 1998; Randrianambinina et al.2003; Rendigs et al.2003; Weidt 2001). Even though not observed in this area, Microcebus murinus possess the ability to hibernate (Schmid 1999; Schmid and Kappeler 1998; Schülke and Ostner 2007). There are interspecific metabolic variations within Microcebus. For instance, whereas Microcebus murinus, M. rufus, M. berthae, and M. ravelobensis all possess the ability to enter daily torpor, only M. murinus and M. rufus have been reported to hibernate (Schmid 1999; Schmid and Kappeler 1998; Schülke and Ostner 2007). Northwestern Madagascar is the only well studied region on the island where Microcebus spp. does not hibernate, which has been explained by relatively high minimum ambient temperatures (Schülke and Ostner 2007).

We here investigate whether females Microcebus murinus and M. ravelobensis occupy different feeding niches and/or reduce their locomotor activity during periods of food shortage, which may reduce interspecific competition over food resources. We focused on females because food is thought to be the most limiting resource for reproductive success in females, but not in males (Trivers 1972). We predict that females of Microcebus murinus and M. ravelobensis should 1) show dietary differences in their use of certain food categories and plant taxa, 2) change their diet composition with seasonal changes in food abundance, 3) show seasonal variations in their dietary overlap, 4) increase their degree of food partitioning during periods of food shortage, or 5) reduce their locomotor activity during periods of food shortage, potentially indicating an energy expenditure reduction.

Materials and Methods

Study Site and Climate

We conducted this study during a total of 11 mo between May 2007 and April 2008 (except February 2008) in the dry deciduous forest in the Ankarafantsika National Park in northwestern Madagascar (135,000 ha), ca. 120 km southeast of Mahajanga. We collected no data during February 2008. The study site was a 30.6 ha area locally known as Jardin Botanique A (JBA) (16ο19′S, 46ο48′E), where Microcebus murinus and M. ravelobensis exist in sympatry. The site is easily accessible via a 50 × 50 m trail grid system. The climate is seasonal and characterized by a relatively cooler dry season from May to October and a relatively warmer rainy season from November to April with heavy rains in January and February.

Data Collection

Trapping and Morphometry

We obtained climate data from the local breeding station of Durrell Wildlife Conservation Trust. Temperature and rainfall data were available for the whole study year, except for rainfall data from February 2008. Based on the seasonal climatic changes (Fig. 1) and the corresponding changes in food abundance (Fig. 2), we separated our study period into 4 seasonal periods: the early part of the dry season (P1: May–July), the late part of the dry season (P2: August–October), the early part of the rainy season P3: November–January), and the late part of the rainy season: (P4) February–April.
Fig. 1

Monthly climatic data from May 2007 to April 2008, grouped into 4 study periods (P1–P4). Monthly temperatures are shown as the mean and range of the minimum and maximum temperature. The total rainfall is shown for each month. We collected no rainfall data in February.

Fig. 2

Seasonal availability of leaves (L), flowers (FL), and fruits (FR) from May 2007 to April 2008 separated into 4 periods (P1–P4). The y-axis shows mean proportions (%, mean of bimonthly estimates) of the amounts of leaves, flowers, and fruits in relation to the maximum possible production of each individual tree. Min = minimum; Max = maximum; and SD = standard deviations are provided for each period below the graph.

We captured mouse lemurs during 1–8 capture nights per month (except December 2007) using 100 Sherman live traps baited with banana at the intersections of the trails (ca. every 50 m). We determined the sex of the trapped individuals and measured them (Hafen et al.1998). We ear-marked new individuals (1–2 small triangular cuts of ca. 2 mm2 in the outer part of the pinna) and injected a unique transponder chip subcutaneously under the dorsal skin (Trovan Small Animal Marking System, Telinject®).

Fecal Samples

From May to October 2007, we collected a total of 52 fresh fecal samples from females during capturing and stored them in 1.5-ml tubes in 90% alcohol. We collected 14 samples from 7 female Microcebus murinus and 8 samples from 5 female M. ravelobensis in P1, and 15 samples from 13 female Microcebus murinus and 15 samples from 5 female M. ravelobensis in P2. We weighed the fecal samples, dissected and visually inspected them under × 20–40 magnification, and counted the number of seeds and animal parts per 0.1 gram of feces at the University of Veterinary Medicine Hanover. When we collected >1 sample for 1 individual during a period, we pooled the samples.

Focal Observations

We equipped 11 female Microcebus murinus and 9 female M. ravelobensis with radiocollars (3 g, TW4-button cell tags, Biotrack, UK) and located focal females via a telemetry receiver with an antenna (TR-4 with RA-14 K antenna; Telonics Inc., Mesa, AZ) and a headlamp (Petzl Myo5 or Petzl Tikka Plus, France). We used a flashlight (Mag-Lite® 3D-Cell), a dictaphone (Olympus digital voice recorder, WS-320 M), and a GPS device (Garmin GPS 60 or Garmin Etrex Vista) to facilitate nightly observations. The observer–subject distance varied from 1 to 15 m. We intended to follow 5 females of each species throughout the whole study, but this was not possible because of recapture failure and predation. For unknown reasons, the capture rate of female Microcebus ravelobensis during the early part of the dry season 2007 was unusually low (compared to 1997 and 1998: Schmelting et al.2000). Instead, we followed 2–7 females per species and period. We conducted focal observations on 113 evenings (10–28 evenings per period) from 17:30 to 22:30 h or 18:00 to 23:00 h (depending on seasonally changing light conditions). We were able to observe the collared individuals for 151 h. We observed Microcebus murinus for 93 h over 53 nights (P1: 26 h/14 evenings, P2: 35.5 h/15 evenings, P3: 23 h/14 evenings, P4: 8.5 h/10 evenings), and M. ravelobensis for 58 h over 60 nights (P1: 8.5 h/10 evenings, P2: 36.5 h/28 evenings, P3: 9.5 h/12 evenings, P4: 4 h/10 evenings). We were able to observe Microcebus murinus for almost twice as long as M. ravelobensis per followed hour, probably owing to higher locomotor activity in M. ravelobensis. Observation conditions changed over the year and were especially low during P4 due to full leaf cover in the rainy season.

We defined a feeding bout as a feeding episode in which an individual was continuously feeding. If the subject interrupted its feeding activity for >20 s, we recorded this as a new feeding bout. We classified feeding bouts into the following food categories: arthropods, reptiles, leaves, insect secretion, gum, fruits, or buds. We recorded a total of 536 feeding bouts, and identified food items for 381 of these (Microcebus murinus: 255, M. ravelobensis: 126). We categorized 28 bouts as arthropods, which we were not able to classify on a lower taxonomic level and therefore sorted into a single arthropod group. We categorized 64 bouts as insect secretion, a sugary secretion produced by flatid leaf bug nymphs (we observed colonies of flatid leaf bug nymphs only during P1–P3). Of the remaining 289 bouts, all of which were plant items (gum, fruits, or buds), we could taxonomically determine 286. We could not determine food items in 1 fruit-feeding event in Microcebus ravelobensis during P1, 2 fruit-feeding events in M. murinus, and 1 leaf-feeding event in M. ravelobensis. There were 4 individuals that we never observed feeding (P1: 2 Microcebus murinus, P3: 1 M. murinus, P4: 1 M. ravelobensis).

We calculated the minimum percentage dietary overlap of the 2 species by summing the minimum percentage overlap of all shared food resources (pij or pik) using the formula: \( \sum {\left( {{\hbox{minimum}}\;{{\hbox{p}}_{{ij}}},{p_{{ik}}}} \right)} *100 \) (Krebs 1989; Renkonen 1938). The scale ranges from 0% to 100%, with 0% indicating no resources in common and 100% indicating complete overlap.

We used 5-min scans to estimate activity budgets of Microcebus murinus and M. ravelobensis, and classified behaviors as feeding, foraging (searching for food), resting (sitting still, without searching for food or feeding), and moving (locomotion). We included only scans recorded after the mouse lemurs had left their daily sleeping site. Owing to low visibility, we sometimes had problems distinguishing between foraging and moving. If this was the case, we recorded moving. Social activities occurred only occasionally and we did not classify them into a separate behavioral category. Instead, based on the underlying body movements, we categorized them as feeding, foraging, resting, or moving. We recorded activity only during the first half of the night. However, previous studies of Microcebus murinus and M. ravelobensis indicate that there are no consistent differences in activity patterns over the course of the night (Reimann 2002). More importantly, no significant interspecific differences in activity pattern were found during different parts of the night (Reimann 2002).

Plant Phenology

To gain information about seasonal changes in plant availability, we collected plant phenology data along four transects (total length ≈ 320 m) located in the study area. We included 272 individual plants, which we marked and identified taxonomically (21 lianas, 37 shrubs, and 214 trees, belonging to 78 genera). We tried to cover all available plant genera along the transects. Fifty-one percent of these plant genera were known feeding plant species of mouse lemurs (Radespiel 2006; Thorén unpubl. data). Twice monthly we monitored the abundance of flowers, leaves, and fruits (both fleshy and nonfleshy), estimated as the percentage of the total capacity of each individual plant. We did not determine plant phenology in mid-August, at the beginning of September 2007, in January, February, or at the beginning of March 2008.

Arthropod Trapping

To investigate the seasonal abundance of arthropods, we trapped arthropods using 6 pitfall traps (3.0-liter buckets), 6 sticky traps (yellow sticky traps, 25 × 32 cm, Neudorff), and 1 light trap (Leuchtfalle 12 V/220 V classic, Bioform Entomology & Equipment). We placed the pitfall traps (dug into the ground with the opening at ground level) and sticky traps (attached to tree trunks ca. 1.5 m above ground) at 6 different points in the study area, and the light trap at 1 point in the middle of the study area. We activated the traps in the late afternoon twice monthly (around the 1st and the 15th each month; d 1 and 3: pitfall and sticky traps, d 5: light trap), and checked them early the next morning. We recorded environmental conditions (moon phase and rainfall) of the capture nights. We lack sticky trap data from the beginning of May and light trap data from mid-May 2007, and overall arthropod capture data from January, February and the beginning of March 2008. We calculated the mean number of specimen trapped per capture session for each period (absolute number of arthropods divided by the number of capture sessions within each period). We excluded the incomplete data set from the beginning and middle of May.

This study was approved by CAFF/CORE, the Department des Eaux et Forêts (DEF), and the Association pour la Gestion des Aires Protégées (ANGAP). All field handling and sampling procedures adhered to the legal requirements of Madagascar and were approved by the Malagasy Ministry of Water and Forests.

Statistical Analyses

We analyzed our results using STATISTICA 6 (StatSoft, Inc. 2004), and set significance for all tests at p < 0.05. To investigate seasonal and interspecific differences in activity pattern and diet, we performed χ2 tests (r × k tables) on the overall absolute frequencies of feeding bouts or scans. We considered significant deviations from expectancy as confirmed if a single cell χ2-value exceeded the level of significance (χ2 = 3.86) for df = 1. Statistical comparisons were not possible on the basis of the individual values because of the small sample size. However, the median, minimum, and maximum proportions of the diet composition and activity for each period are presented in Appendixes 1 and 2. We used the Mann-Whitney U test to investigate interspecific differences in the number of seeds and animal parts per 0.1 g of feces. We could not analyze seasonal differences in the number of seeds and animal parts per 0.1 g of feces because of low sample size.

Results

Dietary Composition

Throughout the study, both female Microcebus murinus and female M. ravelobensis fed on gum, insect secretions, fruits (fleshy as well as nonfleshy), and arthropods (Fig. 3, P1–P4). In addition, only female Microcebus murinus consumed buds, and only female M. ravelobensis fed on leaves and reptiles. The diet of female Microcebus murinus consisted mainly of food items from a single food category in each study period: gum (67.7–78.8%) during P1, P2, and P4, and fruit during P3 (83.3%; Fig. 3). In contrast, the diet of female Microcebus ravelobensis consisted of food items from 2–3 relatively evenly distributed food categories per study period. During P1 and P2, these were gum (30.0–46.6%) and insect secretions (40.9–42.9%); during P3 these were gum (30%), insect secretions (20%), and arthropods (30%); and during P4 these were gum (38.1%) and fruits (42.9%; Fig. 3). These overall results for the different study periods coincided reasonably well with the individual results (medians, Appendix 1). The medians could not be used for statistical comparisons because of small sample sizes.
Fig. 3

Relative proportion (%) of food items consumed by Microcebus murinus and M. ravelobensis during the study. FB = number of feeding bouts; N = number of females.

We found significant interspecific dietary differences during P2 (χ2 = 31.3, df = 9, n = 200, p < 0.001) and P3 (χ2 = 24.0, df = 9, n = 58, p < 0.05), but not during P1 (χ2 = 7.1, df = 7, n = 36, p = 0.42) or P4 (χ2 = 10.0, df = 7, n = 83, p = 0.35.). During P2, female Microcebus murinus fed significantly less (14.3%, χ2 = 5.9) and female M. ravelobensis fed more (40.9%, χ2 = 7.5) on insect secretions than expected. During P3, female Microcebus ravelobensis consumed significantly more insect secretions (20.0%, χ2 = 4.3) and leaves (10.0%, χ2 = 4.0) and less fruits (10.0%, χ2 = 5.2) than expected.

Fecal samples were available from May to October (P1 and P2). All samples except one from Microcebus murinus during P1 contained animal matter. We did not detect any interspecific differences in the number of animal parts per 0.1 g of feces during P1 (Microcebus murinus: n = 7, median = 0.19, range = 0.14–0.48; M. ravelobensis: n = 5, median = 0.17, range = 0.15–0.21; MW U-test: Z = 0.89, p = 0.37); however, during P2 the average number of animal parts was significantly higher in female M. murinus than in female M. ravelobensis (Microcebus murinus: n = 13, median = 0.34, range = 0–0.91; M. ravelobensis: n = 5, median = 0.19, range = 0.14–0.24; MW U-test: Z = 2.52, p < 0.05).

We found seeds in the feces of 3 of 7 female Microcebus murinus and in 3 of 5 female M. ravelobensis during P1. In contrast, we found seeds in the feces of only 1 female Microcebus murinus during P2. The seeds in the feces of female Microcebus murinus belonged to 6 different plant species (P1:5, P2:1), and 5 plant species in female M. ravelobensis (P1:5, P2:0). We found only 1 shared seed type in the feces of both species. We did not detect interspecific differences in the number of seeds in the feces during P1 (Microcebus murinus: n = 7, median = 0, range = 0–0.22; M. ravelobensis: n = 5, median = 0.07, range = 0–0.31; MW U-test: Z = –0.24, p = 0.79) or P2 (Microcebus murinus: n = 13, median = 0, range = 0–0.23; M. ravelobensis: n = 5, median = 0, range = 0–0; MW U-test: Z = 0.26, p = 0.54).

Minimum Percentage Overlap

Female Microcebus murinus consumed plant items from 20 different plant species (4–13 within each period) and female M. ravelobensis from 12 plant species (2–7 within each period, Table I). Shared resources were gum from Astrotrichilia asterotricha (P2), Baudouinia fluggeiformis (P4), Poupartia sylvatica (P1), and Rhapolocarpus similis (P1, P2, P3); insect secretions (P1, P2, P3); fruits from Noronhia boinensis (P3) and Strychnos madagascariensis (P4); and arthropods (P2, P3, P4). During most of the year, both mouse lemur species consumed a considerable proportion of their food plant species exclusively, ranging from 23% (P2) to 56% (P3) in female Microcebus murinus, and from 0% (P1) to 45% (P4) in female M. ravelobensis. Consequently, the diets of the females of both Microcebus murinus and M. ravelobensis overlapped only partially, and the minimum percentage overlap ranging from 26.7% (P3) to 48.5% (P1).
Table I

The relative proportion of food items consumed by Microcebus murinus (mur) and M. ravelobensis (rav) in 4 periods

  

Period 1

Period 2

Period 3

Period 4

  

May–July

August–October

November–January

March–April

Food item

Plant species

mur

rav

mur

rav

mur

rav

mur

rav

Buds

Mammea punctata

  

0.04

     

Rothmania reniformis

  

0.01

     

Fruits

Anacolosa sp.

       

0.05

Baudouinia fluggeiformis

  

0.01

 

0.04

   

Canthium sp.

       

0.3

Crateva simplicifolia

  

0.01

     

Dalbergia sp.

    

0.52

   

Noronhia boinensis

    

0.27

0.1

  

Rothmania reniformis

      

0.15

 

Scolopia inappendiculata

       

0.05

Strychnos madagascariensis

     

0.02

0.05

 

Unknown 1

      

0.02

 

Unknown 2

      

0.02

 

Vitex

      

0.05

 

Gum

Astrotrichilia asterotricha

  

0.04

0.02

  

0.07

 

Baudouinia fluggeiformis

      

0.47

0.4

Bussea perrieri

  

0.01

     

Cedrelopsis microfoliolata

  

0.01

     

Cinnamosma fragrans

   

0.11

    

Commiphora sp.

  

0.01

     

Dalbergia sp.

  

0.04

     

Hazonjia

   

0.03

 

0.2

  

Mystroxylum aethiopicum

0.36

 

0.03

   

0.05

 

Poupartia sylvatica

0.09

0.17

 

0.1

    

Rhapolocarpus similis

0.21

0.33

0.54

0.14

0.06

0.1

0.12

 

Romena

0.09

 

0.04

     

Rothmania reniformis

   

0.03

    

Scolopia inappendiculata

0.03

  

0.02

    

Vahimboay

  

0.02

     

Leaves

Noronhia boinensis

     

0.1

  

Insect secretions

 

0.18

0.5

0.14

0.41

0.02

0.2

  

Arthropods

 

0.03

 

0.04

0.13

0.08

0.3

0.05

0.1

Reptiles

        

0.05

N/FB

 

3/33

2/6

5/112

7/88

3/48

4/10

3/60

3/20

Percentage overlap

   

48.5

33.8

26.7

46.7

  

Percentage overlap = minimum percentage overlap of shared food resources; FB = number of feeding bouts; N = number of females.

Seasonality

Temperatures varied substantially over the year, between the absolute yearly minimum in June during P1 (11.5°C) and the absolute yearly maximum in October during P2 (39.0°C). The average minimum temperature varied between the early and late part of the dry season (P1 and P2). In May, the average minimum temperature was still relatively high after the rainy season, before decreasing and staying relatively low until increasing again after August (Fig. 1). Rainfall varied greatly between P3 and P4 (Fig. 1). Leaves, flowers, and fruits were available year-round, but in varying quantities (Fig. 2). Leaf availability decreased from a mean coverage of 65.9% (P1) to 46.7% (P2), and increased to a maximum of 88.9% in the rainy season (P4). The abundance of flowers and fruits varied, but both peaked during P3.

We captured a total of 2881 arthropods belonging to 19 different taxonomic groups from June 2007 to April 2008 (pitfall trap: 504, sticky trap: 505, light trap: 1872, Table II). In general, we trapped Coleoptera, Hemiptera, Lepidoptera, Diptera, and Arananea most frequently. The mean number of specimens trapped varied from 162 (P3) to 242 (P1). The high mean number of arthropods trapped in P1 can be attributed mainly to 1 capture session at the beginning of June. The majority of these arthropods were captured with the light trap and belonged to the orders of Coleoptera and Diptera (flying insects), but the number of Aranae captured with the pitfall traps was also particularly high during this capture session. This high peak cannot easily be explained by extreme environmental conditions.
Table II

Arthropod phenology

 

P1

P2

P3

P4

P1–P4

 

LT

PT

ST

Total

LT

PT

ST

Total

LT

PT

ST

Total

LT

PT

ST

Total

Total

Absolute no.

679

202

87

968

677

161

151

989

357

77

215

649

159

64

52

275

2881

N

4

6

4

3

17

Mean

170

51

22

242

113

27

25

165

89

19

54

162

53

21

17

92

169

Order

                 

Araneae

 

27.0

3.0

30.0

 

15.0

0.7

15.7

 

5.5

 

5.5

 

3.3

0.7

4.0

14.6

Archaeognatha

 

0.8

 

0.8

 

0.2

 

0.2

        

0.2

Blattodea

2.0

0.3

 

2.3

1.7

0.2

1.5

3.3

0.5

0.3

0.5

1.3

    

2.0

Chilopoda

         

0.8

 

0.8

    

0.2

Coleoptera

66.8

4.8

1.5

73.0

71.5

2.8

2.0

76.3

33.3

5.3

18.0

56.5

21.3

4.7

0.3

26.3

62.1

Dermaptera

2.0

  

2.0

0.2

  

0.2

0.8

  

0.8

 

0.3

 

0.3

0.8

Diplopoda

 

0.5

 

0.5

     

1.3

 

1.3

 

0.3

 

0.3

0.5

Diptera

66.3

 

1.0

67.3

0.5

 

1.3

1.8

0.3

 

0.3

0.5

    

16.6

Hemiptera

15.5

 

12.0

27.5

18.5

0.2

17.2

35.8

13.8

0.3

31.3

45.3

18.0

 

16.0

34.0

35.8

Homoptera

3.0

  

3.0

    

0.5

  

0.5

    

0.8

Hymenoptera

2.0

3.0

3.8

8.8

1.2

2.2

2.3

5.7

 

1.3

1.0

2.3

 

7.3

0.3

7.7

5.9

Isoptera

    

0.3

  

0.3

0.8

  

0.8

   

0.0

0.3

Lepidoptera

10.0

  

10.0

18.7

  

18.7

31.0

 

2.0

33.0

12.0

  

12.0

18.8

Mantodea

  

0.3

0.3

            

0.1

Neuroptera

0.3

  

0.3

    

6.8

  

6.8

    

1.6

Opilones

 

5.8

 

5.8

 

3.5

 

3.5

 

0.3

 

0.3

    

2.6

Orthoptera

2.0

7.8

0.3

10.0

0.3

2.7

 

3.0

1.8

4.5

0.8

7.0

1.7

5.3

 

7.0

6.3

Trichoptera

      

0.2

0.2

        

0.1

Zygentomes

 

0.8

 

0.8

 

0.2

 

0.2

        

0.2

Absolute number (Absolute no.) and mean number (absolute no. divided by N: number of capture sessions) trapped within each period, by type of traps (LT = light trap, PT = pitfall traps, ST = sticky traps) and the mean absolute number of each arthropod order in the respective trap type per capture session.

Dietary composition changed seasonally in female Microcebus murinus (χ2 = 154.9, df = 19, p < 0.001, n = 255) and in female M. ravelobensis (χ2 = 61.9, df = 23, p < 0.05, n = 126) (Fig. 3, Appendix 1). Female Microcebus murinus consumed significantly less fruit than expected during P1 (0%, χ2 = 7.6), less fruit (1.8%, χ2 = 22.1) and more buds (5.4%, χ2 = 4.3) during P2, more fruit (83.3%, χ2 = 75.2) and less gum (6.3%, χ2 = 23.5) during P3, and less insect secretions (0%, χ2 = 5.6) during P4 than expected. Female Microcebus ravelobensis consumed significantly less fruit than expected during P2 (0%, χ2 = 7.7), more leaves (10%, χ2 = 4.5) during P3, and more fruit (42.9%, χ2 = 28.0) and reptiles (4.8%, χ2 = 4.2) and less insect secretions (0%, χ2 = 6.8) during P4. We did not detect any significant differences from the expected values during P1.

Activity Pattern

The proportion of time spent foraging, feeding, moving, and resting changed seasonally in both female Microcebus murinus (χ2 = 141.4, df = 15, n = 979, p < 0.001) and in female M. ravelobensis (χ2 = 52.1, df = 15, n = 623, p < 0.001; Fig. 4, Appendix 2). These overall results for the different study periods coincided fairly well with the individual results (medians, Appendix 2). The medians could not be used for statistical comparisons owing to small sample sizes.
Fig. 4

Activity budgets of Microcebus murinus and M. ravelobensis. n = number of scans, N = number of females.

During P1, female Microcebus murinus spent most of the time resting (72.9%) and showed the annually lowest proportion of scans feeding (9.8%) and foraging (6.7%). Resting decreased continuously from P1 to P4, whereas feeding and foraging increased in parallel. Female Microcebus murinus rested significantly more during P1 (72.9%, χ2 = 27.0), whereas foraging (6.7%, χ2 = 11.4) and feeding (9.8%, χ2 = 22.1) were less frequent than expected. During P2 female Microcebus murinus moved less than expected (7.1%, χ2 = 5.4). During the entire rainy season (P3 and P4), female Microcebus murinus rested less (P3: 33.3%, χ2 = 13.9 and P4: 17.1%, χ2 = 16.4) and foraged more (P3: 24.2, χ2 = 15.0; P4. 25.0%, χ2 = 5.3) than expected. In addition, they moved more than expected during P3 (16.3%, χ2 = 6.6), and fed more than expected during P4 (43.4%, χ2 = 11.4).

We observed less regular changes in activity patterns in female Microcebus ravelobensis. We detected significant differences from the expected distribution only during P1, when the subjects spent significantly fewer scans resting (17.7%, χ2 = 8.6) and feeding (6.5%, χ2 = 4.9), but most of the time foraging (45.2, χ2 = 11.4) and moving (30.7%, χ2 = 9.3).

We found interspecific differences in activity pattern during P1, P2, and P3, but not during P4 (P1: χ2 = 91.2, df = 7, p < 0.001, n = 317, P2: χ2 = 24.9, df = 7, p < 0.001, n = 838, P3: χ2 = 14.9, df = 7, p < 0.05, n = 349). During P1, female Microcebus murinus rested significantly more (χ2 = 5.4) and foraged less (χ2 = 10.2) than female M. ravelobensis (resting: χ2 = 19.3, foraging: χ2 = 41.9). Further, female Microcebus ravelobensis moved more than expected (χ2 = 11.1). During P2, female Microcebus murinus foraged significantly less (χ2 = 6.1) and female M. ravelobensis more (χ2 = 5.5) than expected. Finally, during P3, female Microcebus ravelobensis fed less (χ2 = 5.1) and rested more (χ2 = 3.9) than expected (Fig. 4). Female Microcebus murinus spent 38.2% of scans in P1 and 27.2% of scans in P2 resting inside a tree trunk. During P3 and P4, Microcebus murinus was observed resting only on open substrates such as branches, or on tree trunks. We never observed female Microcebus ravelobensis resting inside tree trunks.

Discussion

Our study revealed dietary differences between female Microcebus murinus and female M. ravelobensis regarding consumed food categories and plant taxa. We found that both of their diets change seasonally. However, seasonality was not equally expressed in the diets of both species, and jointly used food resources were not consumed to the same extent during the same period. In contrast to our prediction, the dietary overlap of female Microcebus murinus and female M. ravelobensis was higher than we expected during the dry season. However, during the early part of this season, females of Microcebus murinus decreased their locomotor activity, which might help to minimize energetic costs.

Food Partitioning

Despite some general dietary similarities between the females of Microcebus murinus and M. ravelobensis, we found signs of feeding niche differentiation. First, in accordance with preliminary feeding ecology data (Radespiel et al.2006), we confirm interspecific differences in dietary composition between female Microcebus murinus and female M. ravelobensis. These differences were expressed mainly in the proportion of insect secretions consumed during the late part of the dry season and the early part of the rainy season (P2 and P3), arthropod consumption during the late part of the dry season (P2), and fruit and leaf consumption during the early part of the rainy season (P3). The exclusive leaf consumption by Microcebus ravelobensis was based on a low sample size, but is consistent with previous accounts (Radespiel 2006), and therefore suggests the existence of a basic dietary difference.

Second, the importance of certain food resources during a specific period differed between the species. Although some food resources were part of the diet of both species, they were not consumed to the same extent during the same time of the year. For instance, gum was available and consumed by both species all year round. However, with increased fruit availability in the early part of the rainy season (P3), female Microcebus murinus drastically reduced gum consumption and consumed fruit almost exclusively. In contrast, even though female Microcebus ravelobensis consumed fruit during this period, fruit accounted for only a minor proportion of the total diet. Instead, the diet of Microcebus ravelobensis during this period consisted of a relatively high proportion of gum as well as of insect secretions and arthropods. However, the high proportion gum consumed by Microcebus ravelobensis during this period was attributed to one single female. Therefore, this result should be treated with caution. The seasonally abundant insect secretions (available from P1, the early part of the dry season, until P3, the early part of the rainy season) were still an important food resource for Microcebus ravelobensis in the early part of the rainy season (P3), but were only of minor importance for M. murinus during this period. In general, the diet of Microcebus murinus showed larger seasonal changes than the diet of its sympatric congener. Similar patterns have also been observed in Microcebus murinus and its congener M. berthae in Kirindy, western Madagascar (Dammhahn and Kappeler 2008b), and may be due to a generally higher plasticity in the feeding regimen of M. murinus.

Third, the diets of female Microcebus murinus and M. ravelobensis were only partially overlapping. Some food categories and plant species were used exclusively by one species, and there were interspecific differences in the proportion of the shared food resources consumed. Female Microcebus murinus had a more diverse diet than its congener, similar to observations from Kirindy (Dammhahn and Kappeler 2008a, b, 2010). However, female Microcebus ravelobensis in Ampijoroa seem to have a wider feeding niche than M. berthae in Kirindy, and consumed considerably more exclusively used food resources.

The dietary overlap of Microcebus murinus and M. ravelobensis was relatively high during the early part of the dry season (P1). It is possible that food shortage forced the 2 species to use the same limited food resources. However, a stable coexistence predicts that species should have evolved strategies to reduce interspecific food competition. The high dietary overlap might instead have been due to relatively high food abundance at this time (P1). The fact that we regularly found seeds in the feces of the mouse lemurs during this period (P1), but not during the late part of the dry season (P2), supports this hypothesis.

Locomotor Activity

We observed reduced locomotor activity in female Microcebus murinus but not in female M. ravelobensis during the early part of the dry season (P1), with increased scan frequencies of resting behavior and decreased scan frequencies of foraging and feeding. In contrast to Microcebus ravelobensis, female M. murinus spent 38.2% of scans resting inside tree trunks during this period of the year. Whether the resting behavior of Microcebus murinus inside the tree trunks coincided with bouts of torpor (reduction of metabolic rate) could not be clarified. Nevertheless, if an animal rests, it refrains from feeding (low caloric input) but also does not spend much energy on locomotion (low caloric output). Thus, it is possible that the decreased locomotor activity in female Microcebus murinus reflects reduced energetic requirements during this energetically demanding period of the year. As a consequence, the potential competition with females of Microcebus ravelobensis over limited food resources may be reduced, allowing dietary overlap to be relatively high in the early part of the dry season (P1). However, the interspecific difference in locomotor activity during P1 should be interpreted with some caution because we observed only 2 female Microcebus ravelobensis during P1, owing to the low capture rate of suitable females. Nonetheless, whether the observed interspecific difference in activity pattern reflects the presence of different energy-saving strategies in Microcebus murinus and M. ravelobensis (Kobbe and Dausmann 2009; Schmid et al.2000), and coincide with interspecific differences in the capability for seasonal tail-fattening (Zimmermann et al.1998), requires further investigation. Females of neither species decreased their locomotor activity during the late part of the dry season (P2), which can best be explained by the onset of the mating season. Females of both species typically enter their first estrus in August/September, leading directly to their first gestation (Randrianambinina et al.2003; Schmelting et al.2000), and they may therefore need to find mates and more food during this time of the year.

Conclusions

This study provides overall support for the existence of feeding niche differentiation between 2 sympatric mouse lemur species. First, we found signs of food partitioning regarding food categories and plant taxa consumed. Second, seasonality was not equally expressed in the dietary composition of females of the 2 species, which indicates that the importance of certain food resources during a specific period was not the same in females of both species. Third, the dietary overlap between the 2 species showed seasonal variations, although the degree of food partitioning did not, as expected, increase during periods of food shortage. However, the unexpectedly high dietary overlap during the early part of the dry season may not lead to high levels of food competition because it seems to coincide with a reduced locomotor activity of female Microcebus murinus. If this reduced locomotor and feeding activity indeed serves to reduce their energy expenditure in the early dry season, this mechanism may further facilitate the coexistence of 2 otherwise ecologically similar mouse lemur species, Microcebus murinus and M. ravelobensis, in Ampijoroa.

Notes

Acknowledgments

We thank the Department des Eaux et Forêts (DEF), the members of CAFF/CORE, the University of Antananarivo (D. Rakotondravony and the late O. Ramilijaona), and the Association pour la Gestion des Aires Protégées (ANGAP) for permission to work in the Ankarafantsika National Park. We also thank the staff of the National Park for their continuous support. We thank Blanchard Randrianambinina, Solofo Rasoloharijaona, and Romule Rakotondravony for their valuable help during the study. Many thanks go to Sonja Kunath, Miriam Linnenbrink, Pièrre Razafindraibe, Fanomezantsoa Rakotonirina, and Roger Randrimparany for their enthusiastic help during data collection. The Durrell Wildlife Preservation Trust is acknowledged for providing the climate data of Ampijoroa. We also thank Albert Melber, who helped with arthropod identification; Roger Edmont for botanical expertise; Angie Faust for proofreading the manuscript; and the editor and 2 anonymous reviewers for helpful comments on the manuscript. All field handling and sampling procedures adhered to the legal requirements of Madagascar and were approved by the Ministry of Water and Forests. We have complied with the ethical standards for the treatment of primates and with the national laws and research rules formulated by the Malagasy authorities.

References

  1. Amarasekare, P. (2003). Competitive coexistence in spatially structured environments: A synthesis. Ecology Letters, 6, 1109–1122.CrossRefGoogle Scholar
  2. Atsalis, S. (1999). Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. International Journal of Primatology, 20, 883–910.CrossRefGoogle Scholar
  3. Azevedo, F. C. C., Lester, V., Gorsuch, W., Lariviere, S., Wirsing, A. J., & Murray, D. L. (2006). Dietary breadth and overlap among five sympatric prairie carnivores. Journal of Zoology, 269, 127–135.CrossRefGoogle Scholar
  4. Bearder, S. K., & Doyle, G. A. (1974). Ecology of bushbabies Galago senegalensis and Galago crassicaudatus, with some notes on their behaviour in the field. PLoS Biology, 109–130.Google Scholar
  5. Behmer, S. T., & Joern, A. (2008). Coexisting generalist herbivores occupy unique nutritional feeding niches. Proceedings of the National Academy of Sciences of the United States of America, 105, 1977–1982.PubMedCrossRefGoogle Scholar
  6. Brown, Jr. W. L., & Wilson, E. O. (1956). Character displacement. Systematic Zoology, 49–64.Google Scholar
  7. Chase, J. M., & Leibold, M. A. (2003). Ecological niches: Linking classical and contemporary approaches. Chicago: University of Chicago Press.Google Scholar
  8. Cox, C. B., & Moore, P. D. (2000). Biogeography: An ecological and evolutionary approach. Oxford: Blackwell Scientific Press.Google Scholar
  9. Dammhahn, M., & Kappeler, P. M. (2005). Social system of Microcebus berthae, the world’s smallest primate. International Journal of Primatology, 26, 407–435.CrossRefGoogle Scholar
  10. Dammhahn, M., & Kappeler, P. M. (2008a). Small-scale coexistence of two mouse lemur species (Microcebus berthae and M, murinus) within a homogeneous competitive environment. Oecologia, 157, 473–483.PubMedCrossRefGoogle Scholar
  11. Dammhahn, M., & Kappeler, P. M. (2008b). Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology, 29, 1567–1589.CrossRefGoogle Scholar
  12. Dammhahn, M., & Kappeler, P. M. (2010). Scramble or contest competition over food in solitarily foraging mouse lemurs (Microcebus spp.): New insights from stable isotopes. American Journal of Physical Anthropology, 141, 181–189.PubMedGoogle Scholar
  13. Dausmann, K. H., Glos, J., Ganzhorn, J. U., & Heldmaier, G. (2004). Hibernation in a tropical primate. Nature, 429, 825–826.PubMedCrossRefGoogle Scholar
  14. Dausmann, K. H., Glos, J., Ganzhorn, J. U., & Heldmaier, G. (2005). Hibernation in the tropics: Lessons from a primate. Journal of Comparative Physiology B, 175, 147–155.CrossRefGoogle Scholar
  15. Fietz, J., & Ganzhorn, J. U. (1999). Feeding ecology of the hibernating primate Cheirogaleus medius: How does it get so fat? Oecologia, 121, 157–164.CrossRefGoogle Scholar
  16. Ganzhorn, J. U. (1988). Food partitioning among Malagasy Primates. Oecologia, 75, 436–450.CrossRefGoogle Scholar
  17. Ganzhorn, J. U. (1989). Niche separation of seven lemur species in the eastern rainforest of Madagascar. Oecologia, 79, 279–286.CrossRefGoogle Scholar
  18. Ganzhorn, J. U., Wright, P. C., & Ratsimbazafy, J. (1999). Primate communities: Madagascar. In J. G. Fleagle, C. Janson, & K. E. Reed (Eds.), Primate communities (pp. 75–89). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  19. Garcia, J. T., & Arroyo, B. E. (2005). Food-niche differentiation in sympatric Hen Circus cyaneus and Montagu’s Harriers Circus pygargus. Ibis, 147, 144–154.CrossRefGoogle Scholar
  20. Gause, G. F. (1934). The struggle for existence. Baltimore: Williams & Wilkins.Google Scholar
  21. Génin, F. (2008). Life in unpredictable environments: First investigation of the natural history of Microcebus griseorufus. International Journal of Primatology, 29, 303–321.CrossRefGoogle Scholar
  22. Hafen, T., Neveu, H., Rumpler, Y., Wilden, I., & Zimmermann, E. (1998). Acoustically dimorphic advertisement calls separate morphologically and genetically homogenous populations of the grey mouse lemur (Microcebus murinus). Folia Primatologica, 69, 342–356.CrossRefGoogle Scholar
  23. Hardin, G. (1960). The competitive exclusion principle. Science, 131, 1292–1297.PubMedCrossRefGoogle Scholar
  24. Hladik, C. M., Charles-Dominique, P., & Petter, J. J. (1980). Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In P. Charles-Dominique, H. M. Cooper, A. Hladik, C. M. Hladik, E. Pages, G. F. Pariente, A. Petter-Rousseaux, A. Schilling, & J. J. Petter (Eds.), Nocturnal Malagasy primates: Ecology, physiology and behaviour (pp. 41–73). New York: Academic.Google Scholar
  25. Houle, A., Vickery, W. L., & Chapman, C. A. (2006). Testing mechanisms of coexistence among two species of frugivorous primates. The Journal of Animal Ecology, 75, 1034–1044.PubMedCrossRefGoogle Scholar
  26. Joly, M., & Zimmermann, E. (2007). First evidence for relocation of stationary food resources during foraging in a strepsirhine primate (Microcebus murinus). American Journal of Primatology, 69, 1045–1052.PubMedCrossRefGoogle Scholar
  27. Kobbe, S., & Dausmann, K. H. (2009). Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge. Die Naturwissenschaften, 96, 1221–1227.PubMedCrossRefGoogle Scholar
  28. Krebs, C. J. (1989). Niche overlap and diet analysis. Ecological methodology (pp. 371–407). New York: HarperCollins.Google Scholar
  29. Lahann, P. (2007). Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. Journal of Zoology, 271, 88–98.CrossRefGoogle Scholar
  30. Lahann, P. (2008). Habitat utilization of three sympatric cheirogaleid lemur species in a littoral rain forest of southeastern Madagascar. International Journal of Primatology, 29, 117–134.CrossRefGoogle Scholar
  31. Mester, S. (2006). Populationsdynamik nachtaktiver Kleinlemuren (Microcebus murinus und M. ravelobensis) in Nordwest-Madagaskar. Doctoral dissertation, University of Veterinary Medicine, Hannover, Germany.Google Scholar
  32. Mittermeier, R. A., Konstant, W. R., Hawkins, F., Louis, E. E., Langrand, O., Ratsimbazafy, J., et al. (2008). Lemur diversity in Madagascar. International Journal of Primatology, 29, 1607–1656.CrossRefGoogle Scholar
  33. Olivieri, G., Zimmermann, E., Randrianambinina, B., Rasoloharijaona, S., Rakotondravony, D., Guschanski, K., et al. (2007). The ever-increasing diversity in mouse lemurs: Three new species in north and northwestern Madagascar. Molecular Phylogeny and Evolution, 43, 309–327.CrossRefGoogle Scholar
  34. Peres, C. A. (1993). Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (S. mystax) tamarins in an Amazonian terra firme forest. Journal of Zoology, 230, 567–592.CrossRefGoogle Scholar
  35. Petter, J. J. (1962). Ecological and behavioural studies of Madagascar lemurs in the field. Annals of the New York Academy of Sciences, 102, 267–281.PubMedCrossRefGoogle Scholar
  36. Pianka, E. R. (1973). The structure of lizard communities. Annual Review of Ecology and Systematics, 4, 53–74.CrossRefGoogle Scholar
  37. Radespiel, U. (1998). Die soziale Organisation des grauen Mausmakis (Microcebus murinus, J. F. Miller 1777). Eine freilandbiologische und labor-experimentelle Studie, Doctoral dissertation, University of Hannover, Germany.Google Scholar
  38. Radespiel, U. (2006). Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In L. Gould & M. L. Sauther (Eds.), Lemur ecology and adaptation (pp. 211–233). New York: Springer.Google Scholar
  39. Radespiel, U., Reimann, W., Rahelinirina, M., & Zimmermann, E. (2006). Feeding ecology of sympatric mouse lemur species in northwestern Madagascar. International Journal of Primatology, 27, 311–321.CrossRefGoogle Scholar
  40. Rakotondravony, R., & Radespiel, U. (2009). Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. American Journal of Primatology, 71, 928–938.PubMedCrossRefGoogle Scholar
  41. Randrianambinina, B., Rakotondravony, D., Radespiel, U., & Zimmermann, E. (2003). Seasonal changes in general activity, body mass and reproduction of two small nocturnal primates: A comparison of the golden brown mouse lemur (Microcebus ravelobensis) in Northwestern Madagascar and the brown mouse lemur (Microcebus rufus) in Eastern Madagascar. Primates, 44, 321–331.PubMedCrossRefGoogle Scholar
  42. Rasoazanabary, E. (2004). A preliminary study of mouse lemurs in the Beza Mahafaly Special Reserve, southwest Madagascar. Lemur News, 9, 4–7.Google Scholar
  43. Rasolofoson, D., Rakotondratsimba, G., Rakotonirainy, O., Rakotozafy, L., Ratsimbazafy, J., Rabetafika, L., et al. (2007). Influences des pressions anthropiques sur les lé-muriens d’Anantaka, dans la partie est du Plateau de Makira, Maroantsetra, Madagascar. Madagascar Conservation and Development, 2, 21–27.Google Scholar
  44. Reimann, W. E. (2002). Koexistenz und Nahrungsökologie von Weibchen des grauen und goldbraunen Mausmakis (Microcebus murinus und M. ravelobensis) in Nordwest-Madagaskar. Doctoral dissertation, University of Veterinary Medicine, Hannover.Google Scholar
  45. Rendigs, A., Radespiel, U., Wrogemann, D., & Zimmermann, E. (2003). Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. International Journal of Primatology, 24, 47–64.CrossRefGoogle Scholar
  46. Renkonen, O. (1938). Statistisch-ökologische Untersuchungen über die terrestrische Käferwelt der finnischen Bruchmoore. Annales Botanici Societatis Zoologicae Botanicae Fennicae Vanamo, 6, 1–231.Google Scholar
  47. Schmelting, B., Ehresmann, P., Lutermann, H., Randrianambinina, B., & Zimmermann, E. (2000). Reproduction of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in north-west Madagascar: first results of a long term study. In W. R. Lourenço & S. M. Goodman (Eds.), Diversité et endémisme à Madagascar (pp. 165–175). Mémoires de la Société de Biogéographie, Paris.Google Scholar
  48. Schmid, J. (1999). Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. Journal of Mammalogy, 749–757.Google Scholar
  49. Schmid, J. (2000). Daily torpor in the grey mouse lemur (Microcebus murinus) in Madagascar: Energetical consequences and biological significance. Oecologia, 123, 175–183.CrossRefGoogle Scholar
  50. Schmid, J., & Ganzhorn, J. U. (2009). Optional strategies for reduced metabolism in gray mouse lemurs. Die Naturwissenschaften, 96, 737–741.PubMedCrossRefGoogle Scholar
  51. Schmid, J., & Kappeler, P. M. (1998). Fluctuating sexual dimorphism and differential hibernation by sex in a primate, the gray mouse lemur (Microcebus murinus). Behavioral Ecology and Sociobiology, 43, 125–132.CrossRefGoogle Scholar
  52. Schmid, J., & Kappeler, P. M. (2005). Physiologieal adaptations to seasonality. In D. K. Brockman & C. P. van Schaik (Eds.), Primate seasonality: Implications for human Evolution (pp. 129–155). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  53. Schmid, J., Ruf, T., & Heldmaier, G. (2000). Metabolism and temperature regulation during daily torpor in the smallest primate, the pygmy mouse lemur (Microcebus myoxinus) in Madagascar. Journal of Comparative Physiology B, 170, 59–68.CrossRefGoogle Scholar
  54. Schülke, O., & Ostner, J. (2007). Physiological ecology of cheirogaleid primates: Variation in hibernation and torpor. Acta Ethologica, 10, 13–21.CrossRefGoogle Scholar
  55. Schwab, D. (2000). A preliminary study of spatial distribution and mating system of pygmy mouse lemurs (Microcebus cf myoxinus). American Journal of Primatology, 51, 41–60.PubMedCrossRefGoogle Scholar
  56. Schwab, D., & Ganzhorn, J. U. (2004). Distribution, population structure and habitat use of Microcebus berthae compared to those of other sympatric cheirogalids. International Journal of Primatology, 25, 307–330.CrossRefGoogle Scholar
  57. Statistica Version 6.1 (2004). StatSoft® Inc., Tulsa, USA.Google Scholar
  58. Sushma, H. S., & Singh, M. (2006). Resource partitioning and interspecific interactions among sympatric rain forest arboreal mammals of the Western Ghats, India. Behavioral Ecology, 17, 479.CrossRefGoogle Scholar
  59. Thalmann, U. (2001). Food resource characteristics in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. International Journal of Primatology, 22, 287–324.CrossRefGoogle Scholar
  60. Trivers, R. L. (1972). Sexual selection and the descent of man. In B. Campbell (Ed.), Parental investment and sexual selection (pp. 136–179). Chicago: Aldine.Google Scholar
  61. Weidt, A. (2001). Ökologie und Sozialbiologie von Weibchen des goldbraunen Mausmakis (Microcebus ravelobensis) während der Trockenzeit in Nordwest Madagaskar. Diploma thesis, Göttingen University, Göttingen, Germany.Google Scholar
  62. Yoder, A. D., Burns, M. M., & Génin, F. (2002). Molecular evidence of reproductive isolation in sympatric sibling species of mouse lemurs. International Journal of Primatology, 23, 1335–1343.CrossRefGoogle Scholar
  63. Zimmermann, E., Cepok, S., Rakotoarison, N., Zietemann, V., & Radespiel, U. (1998). Sympatric mouse lemurs in north-west Madagascar: A new rufous mouse lemur species (Microcebus ravelobensis). Folia Primatologica, 69, 106–114.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Sandra Thorén
    • 1
  • Franziska Quietzsch
    • 1
  • Doreen Schwochow
    • 2
  • Lalandy Sehen
    • 3
    • 4
  • Christopher Meusel
    • 1
  • Kate Meares
    • 1
  • Ute Radespiel
    • 1
  1. 1.Institute of ZoologyUniversity of Veterinary Medicine HanoverHanoverGermany
  2. 2.Department of Ecology and Evolutionary BiologyUniversity of CaliforniaLos AngelesUSA
  3. 3.Institute of ZoologyUniversity of Veterinary Medicine HanoverHanoverGermany
  4. 4.Department of Botany, Faculty of ScienceUniversity of AntananarivoAntananarivoMadagascar

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