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Tsidy, Repahaka sy Fotsife: 15 years research on nocturnal lemurs in the Ankarafantsika National Park, Madagascar1

Tsidy, Repahaka sy Fotsife :15 ans de recherche sur les lémuriens nocturnes dans le Parc National d´Ankarafantsika, Madagascar
Marine Joly

Résumés

Tsidy, Repahaka sy Fotsife from the Malagasy: Mouse lemur, sportive lemur and woolly lemur. "The Ankarafantsika Lemur Project", is based at the field station of Ampijoroa in the National Park of Ankarafantsika in the North-West of Madagascar and is conducted by the Institute of Zoology from the University of Veterinary Medicine Hanover (Germany) in close collaboration with the local universities of Antananarivo, of Mahajanga and Madagascar National Parks (authorities for the management of protected areas in Madagascar). The project started in 1996. The goal is to enhance our knowledge on the adaptation and evolution of a previously neglected group of primates, the nocturnal lemurs, and to contribute to their conservation. Thus, researchers study the diversity, ecology, communication and socio-biology of the nocturnal lemurs. They discovered one new mouse lemur species (Microcebus ravelobensis) in this area. They characterised aspects of the morphometry, genetics, communication, ecology, social traits and recently, cognitive abilities of sympatrically living mouse-sized (Microcebus murinus and M. ravelobensis) and cat-sized lemur species (Lepilemur edwardsi and Avahi occidentalis). Some major results are presented in this article showing the importance of exchanging experience, educating Malagasy students and field guides and joint work with Malagasy partners in order to deepen our knowledge on the biology of endemic species. This knowledge is crucial to establish efficient management plans and thus contribute to the conservation of threatened species.

Tsidy, Repahaka sy Fotsife :15 ans de recherche sur les lémuriens nocturnes dans le Parc National d´Ankarafantsika, Madagascar

Tsidy, Repahaka sy Fotsife en langue Malgache : Microcèbe, Lépilémur et Avahi. Le projet de recherche sur les lémuriens nocturnes d´Ankarafantsika est basé à la station d´Ampijoroa dans le Parc National d´Ankarafantsika dans le nord-ouest de Madagascar. Il est mené par l´Institut de Zoologie de l´Ecole Vétérinaire de Hanovre (Allemagne) en collaboration étroite avec les universités locales d'Antananarivo, Mahajanga ainsi que Madagascar National Parks (autorité chargée de gérer les aires protégées de l´île). Le projet a débuté en 1996. Son but est d´améliorer les connaissances sur l´évolution et l´adaptation d´un groupe de primates souvent négligé, les lémuriens nocturnes, et de contribuer à leur conservation. Pour cela, les chercheurs ont mené de nombreuses études sur la diversité, l´écologie, la communication, la sociobiologie des lémuriens nocturnes dans cette région. Après avoir fait la découverte d´une nouvelle espèce de microcèbe (Microcebus ravelobensis), les chercheurs ont également caractérisé la morphologie, la génétique, l´écologie, la communication ainsi que les aspects sociaux et récemment les capacités cognitives des espèces sympatriques les plus petites (taille de souris ; Microcebus murinus et M. ravelobensis) et de taille moyenne (taille d´un petit chat ; Lepilemur edwardsi et Avahi occidentalis) présentes dans la région. Les principaux résultats de cette collaboration étroite entre les institutions européenne et malgaches sont présentés dans ce chapitre. Ils montrent l´importance d´un échange d´expérience, de l´éducation des étudiants malgaches et des assistants de terrain ainsi que d´un travail commun avec les partenaires malgaches afin de contribuer à l´acquisition des connaissances sur la biologie des espèces endémiques. Ces connaissances sont essentielles pour établir des plans de gestion efficaces et contribuer ainsi à la conservation des espèces menacées.

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Historique

Soumis 15 juillet 2011. Accepté 30 juillet 2011

Texte intégral

1 Introduction

1In 1996 the Institute of Zoology (IfZ) from the University of Veterinary Medicine Hannover established a scientific collaboration with the University of Antananarivo, Madagascar. In 2001, the "Association Nationale pour la Gestion des Aires Protégées" (ANGAP, renamed Madagascar National Parks, MNP, since 2009), Malagasy authority responsible for the management of the protected areas in Madagascar, joined the two partners. Recently, the University of Mahajanga was included in this long-term collaboration. All four collaborators signed a collaboration contract which is renewed every 3-5 years. The goal is to enhance our knowledge on the adaptation and evolution of a previously neglected group of primates, the nocturnal lemurs, and to contribute to their conservation. Up to now, researchers focused on the biodiversity, evolution, ecology and behavioural biology of nocturnal lemur taxa with the publication of more than 50 articles in peer-reviewed and international scientific journals. They participated also in education of local people, environmental protection and species conservation. Most of the research was performed by both the IfZ (mostly German students/scientists but also occasionally French, Dutch, Swiss, Mexican, Swedish, American) and Malagasy students during their internships, Master, “D.E.A.” degree or PhD work. Field experience can be acquired under the supervision of both Malagasy and the IfZ researchers who have several years of experience working on lemurs. Locally, field assistants are hired and contribute to help the researchers in their specific projects. The involvement of local people in the scientific projects further improves their knowledge on the endemic fauna and forest ecosystem and therefore facilitates conservation-directed thinking.

2The IfZ and its partners have several long-term projects taking place mainly in Northwestern and Northern Madagascar but also in the rainforest in the area of Andasibe, Eastern Madagascar. In this article, I will focus on the research performed in the Ankarafantsika National Park (ANP) where the IfZ and partners started their collaboration and initiated the set-up of a long-term field research programme. Eight lemur species actually inhabit the ANP forest: the Coquerel´s sifaka (Propithecus coquereli) is the only diurnal species, the Mongoose lemur (Eulemur mongoz) and the common brown lemur (Eulemur fulvus fulvus) are cathemeral and five nocturnal species: the grey mouse lemur (Microcebus murinus), the golden-brown mouse lemur(Microcebus ravelobensis), the Western fat-tailed dwarf lemur (Cheirogaleus medius), the Milne-edwards's sportive lemur (Lepilemur edwardsi) and the Western woolly lemur (Avahi occidentalis). All species are listed in the IUCN Red List of Threatened Species and classified under the status Least Concern (Microcebus murinus, Cheirogaleus medius), Near Threathened (Eulemur fulvus), Vulnerable (Eulemur mongoz, Lepilemur edwardsi) and Endangered (Propithecus coquereli, Microcebus ravelobensis, Avahi occidentalis; see www.iucnredlist.org/ ). The work of the IfZ and its Malagasy partners focused on nocturnal lemurs and particularly on the two mouse-sized lemurs, the grey and the golden-brown mouse lemur (Figure 1), and the two small cat-sized lemurs, the Milne-edwards's sportive lemur and the Western woolly lemur (Figure 2). In this article, I will present the general characteristics of the ANP, the methods used by IfZ to conduct studies in nocturnal lemurs and what is yet known on the distribution, life history traits, ecology, socioecology, communication and the recent findings on cognitive abilities of these four nocturnal lemur species in the ANP.

Figure 1

Agrandir

Mouse-sized lemurs in ANP : Microcebus murinus (A) and Microcebus ravelobensis (B)
Les lémuriens "à taille de souris" de l ´ANP: Microcebus murinus (A) et Microcebus ravelobensis (B) (crédit: M. Joly)

Figure 2

Agrandir

Cat-sized lemurs in ANP : Lepilemur edwardsi (A) and Avahi occidentalis (B)
Les lémuriens "à taille de chat" de l´ANP: Lepilemur edwardsi (A) et Avahi occidentalis (B).(crédit: M. Joly)

2 Study site and Methods

2.1 The Ankarafantsika National Park

Figure 3

Agrandir

Location of Ankarafantsika National Park in Madagascar and Ampijoroa station with both research areas. Figure legends: A. Location of Ankarafantsika National Park in Madagascar. B. Close up on Ankarafantsika National Park and Ampijoroa Station. Both maps A. and B. are modified from NASA World Wind. C. Aerial photograph from the Ampijoroa Forest Station (Conservation International, 1998) where “JBA” and “JBB”, both research forest patches, are depicted.
Situation géographique du parc national d´Ankarafantsika à Madagascar et de la station d´Ampijoroa et ses deux aires de recherches. Légendes de la figure : A. Situation géographique du parc national d´Ankarafantsika à Madagascar. B. Zoom sur le parc national d´Ankarafantsika et la station d´Ampijoroa. Les cartes A. et B. sont modifiées d´une carte créée grâce au logiciel NASA World Wind. C. Photographie aérienne de la station forestière d´Ampijoroa (Conservation International, 1998) où sont représentées les deux aires de recherche “JBA” et “JBB”.

3The ANP is situated 450 km north of Antananarivo and 115 km South of Mahajanga, in the North-West of Madagascar (Figure 3A). Before becoming a National Park in 2003, this dry deciduous forest area was classified as a “Réserve Naturelle Intégrale” since 1927. The Ampijoroa forest station is situated in the middle of the Park with easy access thanks to the National Road N4 which crosses the Park. Office buildings, accommodations for tourists and a base camp for several scientific research teams are available in Ampijoroa (Figure 3B).

4The forest in Ankarafantsika is typical of the Western domain of Madagascar with a low canopy and many semi-deciduous tree species (Goodman and Benstead, 2006). In Ampijoroa, two forest patches are dedicated to research: the “Jardin Botanique A” (JBA; 16°19’07.2”S, 46°48’35.5”E) and the “Jardin Botanique B” (JBB; 16°18’02.6”S, 46°48’44.7”E) along the Lake Ravelobe (Figure 3C). Both forest patches, 30.6 ha and 5.1 ha respectively, have a 50-m and 25-m grid system respectively which allows an easy spatial orientation in each area. Both research areas were mapped and digitalised by IfZ. In JBA, the substrate is a sandy soil while in JBB plants grow on an argilliferous soil (Sehen et al., 2010). In JBA, trees reach a maximum height of about 16 m and the maximum height in JBB is 22 m (Sehen et al., 2010). Both forest patches are characterised by a high proportion of individual plants with a stem diameter below 10 cm (more than 96.6%; (Sehen et al., 2010)). JBB comprised a higher proportion of large trees, a higher density of lianas, but a lower overall density of plant individuals (Sehen et al., 2010).

5The climate is highly seasonal and characterized by a cool dry season from May to October and a hot and humid rainy season from November to April, with heavy rains in January and February. The mean annual temperature is around 27°C, with an average maximum temperature of about 37°C in October to November and an average minimum temperature of 16°C in June to July. Due to the low rainfall in the dry season and high temperatures throughout the year, many trees loose a large proportion their leaves during the dry season.

2.2 Capture, identification and follow-up of nocturnal lemurs

6During the long-term project, the IfZ and partners have acquired experience in capturing, identifying and following nocturnal lemurs in the forest. According to the species, different capture methods are used. Mouse-sized nocturnal lemurs are easily captured using Sherman live traps (see details on methods and results of capture-recapture in (Zimmermann et al., 1998; Radespiel et al., 2001; Schmelting et al., 2007)). Monthly capture sessions are typically conducted in JBA and JBB and traps are placed at each intersection of the respective trail system. At dusk, the traps baited with a banana piece are installed in the forest between 1.5 and 2 m high in trees or liana tangles. Each trap is controlled on the early morning (or at midnight during the lactation period). All captured animals are either transported back to the camp where they are identified and measured or the same procedure is done in the field. For long-term individual identification, each captured animal is marked with a subcutaneously injected transponder (ID 100, Trovan Small Animal Marking System; Telinject, Römerberg, Germany) and a small (1–2 mm²) tissue biopsy is taken from one or both ears. Morphometrical data are collected routinely (see details in (Zimmermann et al., 1998)). The animals are then released at dusk at their respective capture site. This procedure allowed the maintenance of a long-term database on the mouse lemur population in both research areas.

7According to the position of the sleeping site, small cat-sized nocturnal lemurs are captured using a mist net fastened around the sleeping hole or with a blowpipe using 1 ml cold air pressure narcotic syringe projectiles (see methods for Lepilemur edwardsi: (Rasoloharijaona et al., 2003; Rasoloharijaona et al., 2006; Mendez-Cardenas et al., 2008; Mendez-Cardenas and Zimmermann, 2009) and for Avahi occidentalis: Ramanankirahina et al., in revision). Ketasel 50 (50 mg Ketasel/ml) in the dose recommended by the manufacturers is used as anesthetic. All captured animals are transported back to the camp where they are identified, measured and released back to the forest as described for mouse-sized lemurs.

8Both mouse-sized and cat-sized lemur individuals are regularly followed using radiotelemetry. When captured, individuals are equipped with a cell tag (Biotrack, Dorset, UK) on a radiocollar (TW-4 button cell tag for Microcebusspp : e.g. (Radespiel et al., 2003b), and TW-3 button-cell tag for Lepilemur edwardsi e.g. (Rasoloharijaona et al., 2003) or mounted on a backpack (TW-3 button-cell tag; Avahi occidentalis: Ramanankirahina et al., in revision). This allows to track each individual using a portable receiver (TR-4 with RA-14K antenna; Telonics, Mesa, AZ) and head lamp for locating reflecting eyes of the individual in the vegetation. The use of a Global Positioning System (GPS) enables to record the position of each individual and to map it accurately in the research area using Global Information System softwares (Joly and Zimmermann, 2007; Joly et al., 2008; Thoren et al., 2011b). Note that mouse lemurs move rapidly by running, jumping and clinging in all strata of dense Malagasy forests and tracking them continuously still remains quite challenging.

3 Mouse-sized lemurs in ANP

3.1 Taxonomy

9Mouse lemurs are the smallest lemurs and actually the smallest extant living primates. The taxonomy of the unique genus Microcebus has been completely revised during the past years. Until today, 18 species have been described (Mittermeier et al., 2010). The IfZ and its Malagasy partners contributed to revise the taxonomy of Microcebus by describing a total of 4 new species in Northwestern and Eastern Madagascar (M. ravelobensis: (Zimmermann et al., 1998); M. bongolavensis and M. danfossi: (Olivieri et al., 2007); M. macarthurii: (Radespiel et al., 2008). Two mouse lemur species occur in partial sympatry in Ankarafantsika: the grey and the golden-brown mouse lemur. While the grey mouse lemur (M. murinus) was first described by Miller in 1777 and has a large distribution throughout Western Madagascar, the golden-brown mouse lemur (M. ravelobensis) was only recently described by the research team and its distribution extends beyond the border of the ANP but seems to be restricted to the area between the Betsiboka and the Mahajamba rivers (Olivieri et al., 2007). Both mouse lemur species are morphologically distinct but may be easily confounded during the night. Both colours (as indicated by their names, M. ravelobensis can be distinguished from M. murinus by its brownish head and body fur) and tail length (the golden-brown mouse lemur has a longer tail than the grey mouse lemur; 157 ± 2.53 mm vs 128.4 ± 1.07 mm; (Radespiel et al., 1998; Zimmermann et al., 1998)) are helpful parameters for distinguishing both species. Besides morphometrical differences, both species show genetic differences. Genetic analyses and phylogenetic methods revealed distinct terminal clade and monophyly of both M. murinus and M. ravelobensis (Pastorini et al., 2001; Olivieri et al., 2007; Radespiel et al., 2008).

3.2 Distribution in the ANP

10Microcebus murinus and M. ravelobensis occur in partial sympatry in ANP. Their distribution is unequal in both research areas JBA and JBB: both species are present in JBA while only M. ravelobensis is found in JBB (Zimmermann et al., 1998; Rendigs et al., 2003; Rakotondravony and Radespiel, 2009). In JBA, Sehen et al. captured a total of 32 M. murinus and 24 M. ravelobensis individuals, i.e. the population density can be estimated at about 1 individual/species/ha, while in JBB, 55 M. ravelobensis were captured resulting in a population density of about 11 individuals/ha (Sehen et al., 2010). Microhabitat analyses revealed that in JBA M. ravelobensis were mostly found in microhabitats characterized by a higher percentage of trees with many lianas and a higher cover of the herb layer, whereas M. murinus were found in microhabitats with a higher number of trees with a diameter at breast height greater than 10 cm (Rendigs et al., 2003; Sehen et al., 2010). Moreover, M. ravelobensis was found in similar vegetation structures in JBA and JBB. Two further studies in other areas of ANP confirmed these results: habitats with highest relative abundance of M. ravelobensis were distinct from the sites where M. murinus occurs in sympatry (Rakotondravony and Radespiel, 2009; Sehen et al., 2010). Moreover, Rakotondravony and Radespiel (2009) extended the analysis of relative abundance of mouse lemurs and vegetation structures to 22 different sites in ANP. They found that M. murinus abundance increased with altitude and was highest in dry habitats far from surface water, while M. ravelobensis abundance decreased with altitude and was highest in low altitude habitats close to surface water. M. ravelobensis occurred in more sites and at higher maximum densities than M. murinus and the relative population densities of both species were significantly and negatively correlated with each other. Differences in local and regional distribution patterns between M. murinus and M. ravelobensis are not completely explained yet. However, Rakotondravony and Radespiel (2009) suggest two explanations. First, both mouse lemur species may have different competitive advantages with M. murinus being a superior competitor in drier habitat and M. ravelobensis having advantages living in humid habitats. Second, divergent spatial niches may be explained by past inter-specific competition. However both species seem to have undergone sympatric speciation in different areas of Madagascar. Whereas M. ravelobensis probably speciated Northwestern Madagascar, M. murinus is much more widely distributed in Western and probably only recently colonized the Northwestern Madagascar. Further data are needed to confirm or reject those explanations.

3.3 Life history traits

11Both mouse lemur species show similar life history traits (see Table I). Due to long-term data available on captive M. murinus, its life history is better known than for M. ravelobensis. Data on gestation length and litter size for M. ravelobensis still remain anecdotal. However, both species show a general activity, body mass and reproduction greatly driven by the photoperiod, i.e. by the season (e.g. (Aujard et al., 1998; Perret et al., 1998; Perret and Aujard, 2001; Randrianambinina et al., 2003; Roloff, 2007; Thoren et al., 2011b)). M. murinus and M. ravelobensis are both seasonal breeders (Schmelting et al., 2000; Randrianambinina et al., 2003). In both species, male testes volume increases shortly before the swelling and opening of the female vulva (Schmelting et al., 2000; Wrogemann et al., 2001; Randrianambinina et al., 2003). Testes volume reaches a peak in August and starts to decrease in October (Randrianambinina et al., 2003). Interestingly, in the ANP, M. ravelobensis females enter their first yearly oestrus 4 to 5 weeks earlier than M. murinus(Randrianambinina et al., 2003; Roloff, 2007). While in M. murinus, the reproductive period is triggered by the photoperiod only, in M. ravelobensis, the external temperatures seem to play an additional role for the onset of the reproductive period: the colder the temperatures in July and August, the later the onset was observed (Roloff, 2007). However, M. murinus had a higher conception rate during the first oestrus cycle (Roloff, 2007). Also, female oestrus in M. ravelobensis is not as synchronized as in M. murinus(Randrianambinina et al., 2003). Mouse lemur infants (1 to 3 per litter) are born at the beginning of the rainy season and remain in or close to the sleeping site for the first weeks of their life (Lutermann, 2001; Quietzsch, 2009). Infants usually spend the first 3 to 4 weeks of their life in the maternal nest and start foraging on their own when they are about 8 to 10 weeks old. Female mouse lemurs adopt a parking strategy: they transport dependent infants (up to the age of 6 weeks) out of the nest and leave them, i.e. park them, in a tree while foraging. In Western Madagascar, female M. murinus were observed to groom and nurse related offspring other than their own but transfer only their own offspring (Eberle and Kappeler, 2006). Adoption of related dependent young after their mother’s death was also reported.

Table I

Species

BM

AFR

GL

IBI

LS

NNM

WA

WM

L

murinus

63

0.67

60

3

2

5

40

33

15.5

ravelobensis

56

1

63-69*

1*

Life history traits of both mouse-sized lemur species in ANP (Zimmermann and Radespiel, 2007). All values come from Zimmermann and Radespiel (2007) except for values marked with * issued from Quietzsch (2009). Abbreviations: BM (Body mass): mean body mass (g) of wild adult females; AFR (Age at first reproduction): mean age (years) of first female reproduction, GL (Gestation length): mean gestation length (days), IBI (Interbirth interval): mean interbirth interval (months), LS (Litter size): modal litter size, NNM (Neonatal mass): mean body mass (g) of neonate females, WA (Weaning age): mean age at weaning (days), WM (Weaning mass): mean body mass (g) at weaning, L (Longevity): maximal recorded life span in years.
Traits d´histoire de vie des deux espèces de microcèbes présentes dans l´ANP (Zimmermann et Radespiel, 2007). Toutes les valeurs proviennent de Zimmermann et Radespiel (2007) sauf celles marquées par * qui sont issues de Quietzsch (2009). Abréviations : BM (masse corporelle) : masse corporelle moyenne (g) des femelles adultes sauvages ; AFR (âge lors de la première reproduction) : âge (en années) de la première reproduction pour les femelles, GL (durée de gestation) : durée de gestation moyenne (en années), IBI (intervalle entre deux mises bas) : moyenne de l´intervalle entre deux mises bas (en mois), LS (taille de portée) : taille de portée modale, NNM (masse néonatale) : moyenne de la masse corporelle néonatale pour les femelles (g), WA (âge au sevrage) : âge moyen au sevrage (en jours), WM (masse au sevrage) : masse corporelle moyenne au sevrage (g), L (longévité) : durée maximale de vie enregistrée (en années).

12According to Scheumann et al., Microcebus belong to the high predation risk class with a total of 13 potential predator species (including birds, carnivores, reptiles and primates; Scheumann et al., 2007). Nine of these predator species inhabit the ANP forest. Both Microcebus species in the ANP are assumed to suffer from similarly high predation rates. However, data on survival rate were analysed only for M. murinus yet. Yearly turnover and recapture rates between years varied between 26 and 45 % in M. murinus(Lutermann et al., 2006). No difference was found between males and females which seemed to equally survive to their first breeding season. Survival rates decreased until the second breeding season and only 7% of the females and 14% of the males survived to the onset of the third breeding season. No female lived until a fourth breeding season and only 6% of the males were still alive. The median time to loss of 50% of individuals for both sexes was 10 months only. Most females and males never achieve reproduction (Lutermann et al., 2006; Schmelting et al., 2007).

3.4 Sleeping site ecology

13Sleeping site ecology is crucial for individual survival in small nocturnal lemurs. The quality of a sleeping site indicates the degree of protection from predation and thermal fluctuations. For mouse lemurs, the ideal sleeping site should be of difficult access (e.g., shielded by walls, with a small entrance or inner diameter, or high above ground) to avoid predators and it should provide a buffer against daily temperature fluctuations. Both mouse lemur species show different sleeping site habits in ANP. While M. murinus uses mostly tree holes, M. ravelobensis was found to sleep in a broad variety of less protected sites such as branches, lianas, and were observed to construct leaf nests (Radespiel et al., 2003b; Thoren et al., 2010). Entrance height of the sleeping sites was measured at an average of 2.2 m (± 1.8 m, n=18) for M. murinus and 1.3 m (± 1.3 m, n=12) for M. ravelobensis and no significant difference was found between both species (Radespiel et al., 2003b). Male M. murinus usually sleep alone and frequently change their sleeping sites whereas female M. murinus mostly sleep in groups and show a high site fidelity (Radespiel et al., 1998; Radespiel et al., 2003b). Both sexes of M. ravelobensis sleep in mixed-sex sleeping groups and frequently change their sleeping sites (Radespiel et al., 2003b; Radespiel et al., 2009). For both species, matrilinear relatedness played a major role in the composition of sleeping groups which remains quite stable. In their sleeping sites M. murinus displays a crypsis behaviour whereas M. ravelobensis regularly shows a flight response to the approach of an observer.

3.5 Feeding ecology

14Mouse lemurs are omnivorous and are solitary foragers. In the ANP, both M. murinus and M. ravelobensis feed on exuded gums, insects, fruits, seeds, buds and leaves and show variations in their diet according to the season (Radespiel et al., 2006; Joly-Radko and Zimmermann, 2010; Thoren et al., 2011b). Gum and honeydew, i.e. secretions from homopteran larvae, represent keystone resources during the period of food scarcity for both species (Radespiel et al., 2006; Joly-Radko and Zimmermann, 2010; Thoren et al., 2011b). Both M. murinus and M. ravelobensis are not able to gouge, but collect exuded tree gum by licking and by scraping the bark with the tooth comb (Joly-Radko and Zimmermann, 2010). Assessment of feeding niche in females of both species by focal observations and fecal sample analysis actually revealed only partial dietary overlap (Thoren et al., 2011b). 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. Dietary overlap was affected by the season: the lowest overlap was observed when food was scarce suggesting interspecific feeding niche differentiation when food competition is high. Food competition experiments conducted under standardized conditions actually revealed a difference in competition potential towards food between both mouse lemur species in the ANP: M. murinus showed a higher competitive potential than M. ravelobensis and won more conflicts in the feeding context (encounter between one M. murinus and one M. ravelobensis female were performed in cages; M. murinus showed more aggressive behaviour and M. ravelobensis were more submissive; Thoren et al., 2011a). These results might explain how M. murinus may have expanded geographically despite the presence of other resident local mouse lemur species with the result of a much larger distribution but further investigations are needed to confirm it (Thoren et al., 2011a).

3.6 Mating system and social organization

15As previously mentioned, both M. murinus and M. ravelobensis are nocturnal solitary foragers but often form sleeping groups during the day. Matrilinear relatedness plays a major role in the grouping patterns of both M. murinus and M. ravelobensis(Radespiel et al., 2001; Radespiel et al., 2003a; Radespiel et al., 2009). Their social organization and mating system can be defined as a dispersed multimale/multifemale system with a promiscuous mating pattern (Radespiel, 2000; Weidt et al., 2004). Male but no female dispersal was genetically established in M. murinus (Radespiel et al., 2001; Radespiel et al., 2003a). Young males M. ravelobensis displayed a delayed dispersal behaviour and females were philopatric (Radespiel et al., 2009). During their activity period, high intra- and intersexual home-range overlaps was observed. Individuals of both sexes have spatial access to more than one conspecific of the same and the opposite sex and spatial monopolization of females by certain males have never been observed (Schmelting et al., 2000; Weidt et al., 2004). Male M. murinus adopt a scramble competition strategy (i.e. competitive mate searching): they display ahome range enlargement in mating season (reached a maximum of 4.5 ha, see (Schmelting et al., 2007)) which correlates with the number of accessible females (female home range size is about 1 ha during the mating season, see (Joly and Zimmermann, 2011)). Males also show experience-dependent reproductive tactics. Resident males, which have a better spatial knowledge of resources, mates and potential threats, have higher probabilities to meet mates and therefore reproduce more successfully than new males (Schmelting et al., 2007).

3.7 Communication

16While an enhanced visual system and a reduced olfactory system are generally considered to be a general trend in primate evolution, mouse lemurs (and most of the nocturnal prosimians) possess a still functional vomeronasal organ in addition to the main olfactory system which suggests that they rely heavily on olfactory signals (Schilling, 1979; Barton, 2006). Standardized experiments on gray mouse lemurs indeed demonstrated that mouse lemurs rely on volatile olfactory signals to discriminate and find food as well as to recognize predators (Joly et al., 2004; Siemers et al., 2007; Sundermann et al., 2008; Kappel et al., 2011). Further field investigations on M. ravelobensis revealed that animals display marking behaviour during dispersal (e.g. urine-washing at sleeping sites) and confirmed the importance of olfactory signals as a mechanism to regulate the distribution of different groups in space (Braune et al., 2005). Mouse lemurs not only have an adapted anatomy and high sensitivity for olfactory signals, but also own large mobile ears and exhibit a high auditory sensitivity (Niaussat and Petter, 1980), are highly vocal and show a rich repertoire of social calls (Zimmermann, 1995; Zietemann, 2001; Braune et al., 2005), extending to the ultrasonic range, which is comparable to communication calls of microchiropteran bats, cetaceans, some rodents and some frogs (see (Zimmermann, 1995; Braune et al., 2008). Vocalizations range between about 0.5 kHz to about 36 kHz. Eight major structurally different vocal patterns can be discriminated and different types of social calls are used in contexts such as social cohesion (e.g. trill), attention and alarm (e.g. whistle), or agonistic situations (e.g. tsak; Zimmermann, 1995). The comparison of male advertisement calls between M. murinus and M. ravelobensis revealed species-specific differences as well as differences in response behaviour to playbacks (Braune et al., 2008). Conspecific calls evoked the strongest responses in tested individuals, and sympatric heterospecific advertisement calls evoked lower responses than allopatric heterospecific calls. This was not true for the category of whistle call, mainly used in attention or alarm context (Braune et al., 2008). These results show that social calls may represent an “efficient premating isolation mechanism contributing to species cohesiveness in sympatrically living species” (Braune et al., 2008). Lastly, a field study on M. ravelobensis showed that the call type trill carries group-specific signatures and is mainly used by sleeping group members during reunions. These results suggest that acoustic signals play a major role for intra-group cohesion and coordination (Braune et al., 2005).

3.8 Cognition

17Recently, the IfZ started to investigate the cognitive abilities of mouse lemurs, representing the most ancestral primate condition. While cognitive abilities have been thoroughly investigated in monkeys and apes (Tomasello and Call, 1997), knowledge on physical and social cognition of prosimians remain quite sparse (see (Fichtel and Kappeler, 2010) for a review). Recent studies encouraged the rigorous analysis of observational data of species-specific challenges that require particular cognitive abilities in order to give evidence of the underlying mechanisms (Janson and Byrne, 2007; Byrne and Bates, 2011). In the line with this new approach, the IfZ and its partners aim to understand how mouse-sized lemurs search for food in the forest of the ANP. Most mammals are small and nocturnal, but only few can be studied as individuals ranging in large-scale space. Mouse lemurs are a valuable exception. Using observational data, the IfZ revealed that, especially during the scarce dry season, mouse lemurs revisit the same feeding sites regularly and show preferred direction when leaving their nest (Joly and Zimmermann, 2007). The IfZ therefore initiated and developed the use of feeding platforms to conduct standardized experiments in natural condition and demonstrated that mouse lemurs also selectively revisit baited platforms (Joly et al., 2008), suggesting that mouse lemurs remember where they may find food. Based on this knowledge, the IfZ inferred that mouse lemurs should adopt a strategy to cope with the harsh environmental condition in the ANP that may require enhanced cognitive abilities for planning routes and visits to keystone food resources such as gum trees or sites with homopteran larvae (see §3.4). Indeed, rigorous mathematical analysis of observational data revealed that female M. murinus oriented their travel (average distance of the travel per half-night: 462 m) to an out-of sight food site which coincided with a directional change in their routes, passed other available resources when reaching this first regularly visited food site, and that they travelled to this site more efficiently than using a parsimonious strategy such as a straight travel in a random direction (Joly and Zimmermann, 2011). Such findings suggest that mouse lemurs, mouse-sized nocturnal and solitary ranging mammals with small brains, may plan their route to an out-of-sight target. These results challenge previous statements on the coevolution of spatial cognitive skills, sociality and relative brain size and suggest that ecological pressures actually play a greater role in the evolution of cognitive skills than formerly suggested.

4 Cat-sized nocturnal lemurs in Ankaranfantsika

18Two small cat-sized nocturnal lemurs inhabit the forest of the ANP: the Milne-edwards's sportive lemur (Lepilemur edwardsi) and the Western woolly lemur (Avahi occidentalis). Far less is known about these two species than about mouse lemurs. In general, knowledge on distribution, biology, socioecology and communication of sportive and woolly lemurs is still limited since only a few studies have been conducted so far (however see (Warren, 1997; Warren and Crompton, 1997a; b; Thalmann and Geissmann, 2000; Thalmann, 2001; Rasoloharijaona et al., 2003; Thalmann and Geissmann, 2005; Rasoloharijaona et al., 2006; Rasoloharijaona et al., 2008; Rasoloharijaona et al., 2010). In the following paragraphs I will present the actual knowledge and compare different aspects on their distribution, social behaviour, sleeping site ecology, feeding ecology and communication.

4.1 Taxonomy and distribution

19Sportive lemurs (Lepilemuridae) belong to the Lepilemuridae family and to the unique genus Lepilemur. Twenty-six different species are currently recognized (Mittermeier et al., 2010). Our actual knowledge on sportive lemurs suggests interspecific differences in morphology (Rasoloharijaona et al., 2003; Rasoloharijaona et al., 2008), genetics (Andriaholinirina et al., 2006; Craul et al., 2007) and behavioral aspects (Rasoloharijaona, 2001). The IfZ and its Malagasy partners contributed to revise the taxonomy of Lepilemur (Andriaholinirina et al., 2006) and described a new species in the Northwestern Madagascar: Lepilemur otto (Craul et al., 2007). The Milne Edwards’ sportive lemur (Lepilemur edwardsi) exclusively inhabits the Western dry deciduous forests and has a limited distribution around ANP, from North of the Bestiboka river to the Bay of Loza and the Mahajamba river (Mittermeier et al., 2010).

20Woolly lemurs are the only nocturnal members of the Indriidae and all belong to the unique genus Avahi. Until now, 9 species are recognized (Mittermeier et al., 2010). The Western woolly lemur (Avahi occidentalis) has a restricted distribution, as Lepilemur edwardsi, and lives in the dry deciduous forests from North and East of the Betsiboka River to the Bay of Narinda in Northwestern Madagascar (Mittermeier et al., 2010).

21In the ANP, both species are present in JBA (Warren and Crompton, 1997a; Thalmann, 2001; Rasoloharijaona et al., 2003). However although several censuses and observations were conducted, Avahi occidentalis was never confirmed in JBB (Rasoloharijaona, Rabesandratana, Randrianambinina and Radespiel, unpublished data).

22The population density of L. edwardsi in JBA is about 5 individuals/ha (Rasoloharijaona, 2001). The home range size is about 1 ha (0.98 ± 0.4 ha females and 1.01 ± 0.25 ha for males; (Rasoloharijaona et al., 2006). Density of Avahi occidentalis in JBA was estimated between 2.2 and 2.9 individuals/ha (Marquart, 2002). Their home ranges in JBA varied between 1 and 2 ha (Warren and Crompton, 1997a).

4.2 Life history traits

23Both Lepilemur edwardsi and Avahi occidentalis weigh about 1 kg and no sex differences are found (Lepilemur edwardsi: 934 g in (Zimmermann and Radespiel, 2007); Avahi occidentalis: 999 g in Ramankirahina et al, in revision). Both are vertical clingers and leapers (Warren, 1997; Warren and Crompton, 1997b). Few information on their life history traits are available (Zimmermann and Radespiel, 2007). In both species, reproduction period is seasonal and mean litter size is one (Rasoloharijaona et al., 2000; Zimmermann and Radespiel, 2007).

24According to Scheumann et al., Lepilemur and Avahi belong to the medium predation risk class with a total of 7 and 5 potential bird or carnivore predator species, respectively (Scheumann et al., 2007). Respectively, six and four of these predator species inhabit the ANP forest.

4.3 Sleeping site ecology

25Sportive lemurs in ANP are found to sleep in tree holes in dead or live trees. They are found at an average height of 4.38 m above the ground (Rasoloharijaona et al., 2003). The availability of suitable shelters has been suggested to influence with the distribution of the Milne-Edwards’ sportive lemur (Rasoloharijaona et al., 2003; Rabesandratana, 2006). Pairs typically use a very limited number of suitable sleeping holes in their home range. Pairs use these sites exclusively and defended them jointly against neighbours and strangers by loud call displays (Rasoloharijaona et al., 2006). In contrast, Avahioccidentalis sleeps in trees with dense foliage at heights between 3.5 and 13 m (Warren and Crompton, 1997a). Ramanankirahina et al. (in revision) showed that seasonality affects the sleeping site characteristics (e.g. height) and usage in Avahioccidentalis.

4.4 Feeding ecology

26Both Lepilemur and Avahi of the ANP exclusively feed on leaves and plants and their dietary composition changes seasonally. However a clear differentiation in dietary selection was demonstrated between both species (Thalmann, 2001). Niche overlap is absent during the scarce dry season. Food resources of Avahi consist of relatively rare but large-sized resources such as young leaves and flowers that are of better quality compared to those consumed by Lepilemur. Lepilemur feeds onmoreubiquitous and evenly-distributed mature and old leaves. This dietary specialisation may have shaped the evolution of the different social systems present in both species (see 4.2) and may explain the monogamous social organization in Avahi occidentalis. The narrow food niche may restrict ranging activities of males which could be unable to spatially access more than one receptive female (Thalmann, 2001). The mean distance travelled each night was 340 ± 70 m in Lepilemur and 1170 ± 350 m in Avahi (Warren and Crompton, 1997a). The narrow but high-quality food niche of Avahi may suggest that suitable resources may have to be known exactly for repeated use. Future studies will test whether this species-specific challenge may have enhanced the evolution of better cognitive resources such as spatial memory skills in Avahi than in Lepilemur.

4.5 Mating system and social organization

27Lepilemur edwardsi lives in dispersed male–female pairs (Rasoloharijaona et al., 2000; Rasoloharijaona, 2001; Rasoloharijaona et al., 2003; Rasoloharijaona et al., 2006; Thalmann, 2006). Individuals usually forage alone at night, but establish long-term pairs (Rasoloharijaona et al., 2003). Pair partners share a home range with suitable sleeping and feeding sites, usually sleeping together in the same sleeping site and using home ranges exclusively (Rasoloharijaona et al., 2003; Rasoloharijaona et al., 2006).

28Avahi occidentalis lives in gregarious family groups formed by a pair and its immature offspring (Warren and Crompton, 1997a; Thalmann, 2001). They establish long-term groups and sleep mostly together during the day. Pair partners are usually both travelling and feeding together (Warren and Crompton, 1997a).

4.6 Communication

29Lepilemur edwardsi are highly vocal. Nine structurally different call types have been distinguished (Rasoloharijaona, 2001; Rasoloharijaona et al., 2006). Vocalizations were shown to carry signatures for sex, individual and pair identity (Rasoloharijaona et al., 2006; Mendez-Cardenas and Zimmermann, 2009). They range between about 0.2 kHz to about 6 kHz (Rasoloharijaona, 2001). Pairs use duetting as a vocal display for signalling territory ownership and thus reduce direct aggressive encounters with neighbours and strangers (Rasoloharijaona et al., 2006; Mendez-Cardenas and Zimmermann, 2009). Lepilemur edwardsi emit loud calls mostly during feeding events and in the vicinity of their sleeping sites (Rasoloharijaona et al., 2006; Rasoloharijaona et al., 2010). Investigations from ten different local populations in ANP showed that the vocal activity of L. edwardsi was not affected by population density (Rabesandratana, 2006). Marking behaviour in Lepilemur edwardsi was reported on rare occasions when the animal climbed down a trunk before urinating and defecating (Warren and Crompton, 1997a).

30Little is known on the communication of Avahioccidentalis. Warren and Crompton reported that long-range calling was very limited and only two distinct types of calls were described (Warren and Crompton, 1997a). The piercing ‘ava-hee’ call type, gives them their genus name, and is produced by both sexes. The second call type was a relatively quiet purring made by the vibration of the nostrils. This gentle purring was mainly produced when the animals were in proximity or together. The IfZ is currently revising the vocal repertoire and analysing the emission context of each call type in Avahioccidentalis using its long-term database. Western woolly lemurs have scent glands under the chin, more conspicuous in the males than in females, but marking behaviour has been observed only rarely (Warren and Crompton, 1997a).

5 Conclusions

31This review on the results acquired during the long-term collaboration between the IfZ and its Malagasy partners shows the variety of studies conducted in the ANP on nocturnal lemurs during the last 15 years. Distribution, morphology, life history traits as well as aspects on sleeping site and feeding site ecology, sociality, communication and cognitive abilities have been characterized in mouse-sized and small cat-sized nocturnal lemurs. Both mouse-sized and cat-sized lemurs are adapted to the high predictable and seasonal environment of the ANP. All four species display a seasonal reproduction which allows them to give birth to offspring during the period of food abundance. Both mouse-sized and cat-sized species also face to the limited availability of suitable sleeping sites. Large trees are in a limited amount in the ANP forest and tree holes can be monopolized. Tree holes are mostly used by M. murinus and Lepilemur edwardsi while M. ravelobensis and Avahi occidentalis use nests or sleep in open vegetation and are thus potentially more exposed to predators. According to the sleeping site characteristics, lemurs may also show behavioral flexibility (e.g. flight behavior vs. crypsis behavior while in a hole or nest) and therefore increase their survival rate. Further comparative studies on communication and cognition are still needed, particularly for cat-sized lemurs. It will help for example to understand communication in species living in dispersed vs. cohesive pair system and cognitive challenges encountered by species differing in their diet specialization. All this knowledge is crucial to enhance our understanding on the adaptation and evolution of nocturnal lemurs and further to preserve suitable habitats for the survival of those threatened nonhuman primate species. ANP is the only National Park where M. ravelobensis, Lepilemur edwardsi and Avahi occidentalis occur. Preserving such protected areas is essential to maintain the unique and rich biodiversity of Madagascar which is unfortunately threatened by a continuing loss of habitats for slash-and-burn agriculture, wood extraction, local pet trades and hunting. Few quantitative data on anthropogenically-caused threat on lemur population are available but recently lemur hunting in ANP was documented (Garcia and Goodman, 2003). Garcia and Goodman gathered and identified bone remains of wild animals hunted by local raffia harvesters in ANP. They found the rest of four of the lemur species (Propithecus verreauxi, Eulemur fulvus, Lepilemuredwardsi and Avahi occidentalis). The most common species found in the bone rests correspond to the large diurnal species which represent greater protein sources for human than the other lemur species. They were killed using weapons, e.g. guns. Because of their sleeping site ecology (see 4.3), Lepilemuredwardsi and Avahi occidentalis can be picked up by hand without weapons quite easily. Both mouse lemur species are probably too small to represent a great food source for humans. Since Lepilemur and Avahi can not be maintained and bred in captivity, continuous and long-term monitoring of the forest is of utmost importance to guarantee their conservation. Numerous ongoing projects of the IfZ will contribute to keep on monitoring local populations of nocturnal lemurs in Northwestern Madagascar, propose management plans and to create new protected areas as well as to increase our knowledge on the comparative biology of the numerous newly described species.  

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Notes

1  This long-term project was initiated and supervised by Elke Zimmermann, head of the IfZ. I greatly thank her for having given me the opportunity to work in this long-term project and for her comments on this review. I also thank two anonymous as well as Ute Radespiel, a former PhD student at the IfZ and now senior lecturer at the IfZ and head of the working group “Behavioural ecology and conservation genetics“ for their comments on a previous version of this manuscript. Ute Radespiel as well as Blanchard Randrianambinina and Solofonirina Rasoloharijaona, former PhD students at the IfZ and the University of Antananarivo and now lecturers and researchers at the University of Mahajanga, conducted and co-supervised most of the fieldwork. The PhD work of Andriatahiana Rabesandratana and Romule Rakotondravony, both from the University of Antananarivo and the IfZ and now lecturers and researchers at the University of Toliara and Mahajanga, respectively, and of Barthel Schmelting, Heike Lutermann, Petra Ehresmann, Wiebke Reimann, Pia Braune, Gillian Olivieri, Mathias Craul, Maria Mendez-Cardenas, Lalandy Sehen (University of Antananarivo and IfZ), Franziska Quietzsch and Sandra Thorén as well as the undergoing work of Rindrahatsarana Ramanankirahina from IfZ formed the scientific basis of this review. This long-term project was only possible due to the active participation of numerous undergrad students and field assistants from the University of Veterinary Medicine Hanover, the University of Antananarivo, the University of Mahajanga and the staff of Madagascar National Parks (former ANGAP). The Malagasy authorities gave their authorization to perform the long-term collection of all data. All studies complied with the current laws of Madagascar. The long-term project was financially supported by the German Research Foundation (DFG), the Volkswagen foundation (VW) as well as the German Academic Exchange Service (DAAD).

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Référence électronique

Marine Joly, « Tsidy, Repahaka sy Fotsife: 15 years research on nocturnal lemurs in the Ankarafantsika National Park, Madagascar », Revue de primatologie [En ligne], 3 |  2011, document 10, mis en ligne le 17 mai 2011, Consulté le 25 avril 2014. URL : http://primatologie.revues.org/758 ; DOI : 10.4000/primatologie.758

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Auteur

Marine Joly

Institute of Zoology, University of Veterinary Medicine Hannover, Buenteweg 17, D-30559 Hannover, Germany
Author for correspondence:
marine.joly@tiho-hannover.de

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