Institute of Zoology University of Veterinary Medicine Hannover ______

Comparative feeding ecology of two sympatric mouse lemurs (Microcebus spp.) in northwestern Madagascar

THESIS Submitted in partial fulfillment of the requirements for the degree

DOCTOR OF PHILOSOPHY (PhD) at the University of Veterinary Medicine Hannover

by Sandra Ingrid Kristina Thorén Gothenburg, Sweden

Hannover 2011 Supervisor: Prof. Dr. Ute Radespiel Institute of Zoology University of Veterinary Medicine Hannover Hannover, Germany

Advisory Commitee: Prof. Dr. Hansjoakim Hackbarth Institute of Animal Welfare and Behaviour University of Veterinary Medicine Hannover Hannover, Germany

PD Dr. Björn Siemers Institute of Ornithology Max Planck Insitiute Seewiesen, Germany

1st Evaluation: Prof. Dr. Ute Radespiel Prof. Dr. Hansjoakim Hackbarth PhD Dr. Björn Siemers

2nd Evaluation: Prof. Dr. Jörg Ganzhorn Institute of Zoology University of Hamburg Hamburg, Germany

Date of final exam: 13th of May 2011

To my family

Table of contents

Table of contents

Chapter 1. General introduction ...... 1

1.1 Stable coexistence of species ...... 2 1.2 Biogeographic patterns in species ...... 4 1.2.1 Local abundance ...... 5 1.2.2 Body size...... 6 1.2.3 Climatic variability (“Rapoport’s rule”) ...... 7 1.2.4 Biogeographic history ...... 7 1.2.5 Ecological plasticity ...... 8 1.2.6 Competitive ability ...... 8 1.3 Biogeographic rules in primates ...... 9 1.4 The lemurs of Madagascar ...... 11 1.5 Animal models: the gray mouse lemur (Microcebus murinus) and the golden-brown mouse lemur (M. ravelobensis) ...... 13 1.6 Aim of study ...... 17 1.6.1 Resource use & characterization of feeding niches (Chapter 2) ...... 17 1.6.2 Interspecific food competition (Chapter 3) ...... 18 1.7 References...... 19

Chapter 2. First study 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 ...... 29

2.1 Abstract ...... 30

Chapter 3. Second study Different competitive potential in two coexisting mouse lemur species in northwestern Madagascar ...... 31

3.1 Abstract ...... 32

Chapter 4. Third study Can the distribution of key food plants explain the varying abundance of two mouse lemur species (Microcebus spp.) in northwestern Madagascar? ...... 33

4.1 Abstract ...... 34 4.2 Introduction...... 35 4.3 Methods ...... 36 4.3.1 Study sites ...... 36 4.3.2 Feeding data ...... 38 4.3.3 Botanical data ...... 38 4.3.4 Identification of potential key resources ...... 39 4.3.5 Linkage between key resources, presence and abundance of mouse lemurs ...... 40 4.4 Results ...... 40 4.4.1 Potential key feeding plants ...... 40 4.4.2 Relationship between potential key resources, presence and relative abundance of mouse lemurs .... 42 4.5 Discussion ...... 47 4.5.1 Do mouse lemurs possess key food plants? ...... 47

Table of contents

4.5.2 What other factors might influence the varying abundance of M. murinus and M. ravelobensis in northwestern Madagascar? ...... 49 4.5.3 Conclusions ...... 50 4.6 Acknowledgements ...... 50 4.7 References...... 51

Chapter 5. General discussion ...... 55

5.1 Resource use (Chapter 2 & 4) ...... 56 5.1.1 Implications for coexistence ...... 56 5.1.2 Implications for varying regional abundance & geographic range size ...... 58 5.2 Interspecific food competition (Chapter 3) ...... 61 5.2.1 Implications for coexistence ...... 62 5.2.2 Implications for varying regional abundance & geographic range size ...... 63 5.3 Conclusions...... 64 5.4 References...... 65

Chapter 6. Summary ...... 71

Chapter 7. Zusammenfassung ...... 75

Declaration ...... 79

Chapter 8. Acknowledgements ...... 81

Chapter 9. Curriculum Vitae ...... 85

1

General introduction

1 Chapter 1 General introduction

1.1 Stable coexistence of species

Approximately two million different species of organisms have been described worldwide so far. Each species belongs to a particular ecosystem, which is defined as a biological environment that includes all living organisms (biotic factors) as well as their physical environment (abiotic factors) in a given area (Hutchinson. 1957). The number of different species that can occur in one specific region varies greatly. Well-known areas for species diversity are the Amazon basin and other tropical areas in Africa and southeast Asia (Cox & Moore 2000). The highest species richness of mammals is found in northern South America, especially in the Amazonian lowlands, the Andes, east Africa, and southeast Asia (Ceballos & Ehrlich 2006). Species in a given ecosystem typically possess ecologically different niches. A niche describes the full range of environmental conditions (biological and physical) that is required for the existence of an organism (Hutchinson 1957). Since closely related species of the same taxonomic group are likely to resemble each other due to a shared ancestry, they are also more likely to have highly overlapping niches compared to species of different taxonomic groups (Harvey & Pagel 1991). It has been proposed that two species that are identical should not be able to coexist in the same region. Instead, they are predicted to compete until one species becomes locally extinct (review in Amarasekare, 2003; Brown & Wilson 1956; Chase & Leibold 2003; Gause 1934; Hardin 1960). Therefore, sympatric congeners should have the highest potential to compete for the same essential resources, which may explain why coexisting species in a region usually belong to different taxonomic groups (Hardin 1960). According to the “competitive exclusion principle”, it is sufficient that one species has a slight advantage over another species for this species to dominate in the long term (Hardin 1960). Consequently, for species to be able to stably coexist, they should show some degree of niche differentiation to avoid or reduce interspecific competition for essential resources (review in Amarasekare, 2003; Brown & Wilson 1956; Chase & Leibold 2003; Gause 1934; Hardin 1960). Niche differentiation can be achieved in several ways. For instance, it can result from resource partitioning of two species. Essential resources that can be partitioned include food, space, water, sleeping sites, etc. Differentiated utilization of food resources by sympatric congeners will be further investigated in this doctoral thesis, and has been suggested to enable coexistence in numerous sympatric species (arthropods: Behmer & Joern 2008, invertebrates:

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Pianka 1973, birds: Garcia & Arroyo 2005, mammals: Azevedo et al. 2006; Sushma & Singh 2006). Food partitioning can be expressed in different ways. First of all, competing species might use the same set of food resources but to a different extent. For instance, even though three sympatric primate species in Bolivia showed dietary overlaps, the relative proportion of jointly used food resources in their total diet differed between species (Porter 2001). Second, food resources might be temporally partitioned, which means that shared resources are used at different times. Different species might utilize the same resources but during different times of the day, or alternatively, during different seasons. This can be illustrated by the diurnal versus the nocturnal feeding patterns of different lemurs in Madagascar (Petter 1962). Another example of notable differences in daily activity pattern was observed in two sympatric species of foxes in Brazil, where one species was significantly more nocturnal than the other (Vieira & Port 2007). Third, food resources might be spatially partitioned. The same resources may then be used by competing species, but these species occupy different areas or habitats. Spatial separation of resources can occur on a local scale as well as on a larger geographic scale. A good example is given by two mouse lemur species, Microcebus murinus and M. berthae in western Madagascar. These two species show a high degree of dietary overlap, but their coexistence seems to be facilitated by a spatial separation on a local scale (Dammhahn & Kappeler 2008a, 2008b). A second type of niche differentiation is the “conditional differentiation“, which can occur when species exist in a spatially heterogeneous environment. A landscape that is defined as heterogeneous is characterized by variations in the landscape in terms of biotic and abiotic factors (Amarasekare 2003). Interspecific differences in the ability to use certain resources might depend on varying environmental conditions: One species might be the best competitor for the shared resources in a certain habitat, whereas the other species might be the best competitor in another type of habitat (Amarasekare 2003). Another mechanism that may facilitate the coexistence of species is the trade-off between a higher competitive ability of specialized locally rare species and higher dispersal/colonization in widespread generalists (Levins & Culver 1971; Tilman et al. 1997). This mechanism predicts that successful colonists could suffer from a trade-off in competitive ability and should consequently be constrained to be generalist, whereas locally rare species should be strong competitors and can defend a more specialized diet. Alternatively, species may be restricted by natural enemies and not by available resources. High predation might limit densities of

3 Chapter 1 General introduction competing species reducing or completely eliminating interspecific competition for essential resources (review in Amarasekare, 2003) One of the central questions in the field of community ecology is whether observed niche differences are the outcome of ongoing or historical interspecific competition, or whether they are the result of independent evolutionary pathways and adaptations in different historical environments (overview in Townsend et al. 2002). Another central question is how much the ecological niches of species really need to differ for them to stabily coexist (Armstrong & McGehee 1980; Hutchinson 1959). Most predictions on competitive exclusion have been based on theoretical models. For instance, one well-known model is the “Lotka-Volterra equation” that describes the dynamics of biological systems in which two species, one predator and its prey, interact (Armstrong & McGehee 1980). Theoretical models are useful tools for understanding biological processes, but they are always limited by the assumptions they are based on. For instance, the “Lotka-Volterra model” makes a number of assumptions about the environment and evolution of predator and prey, e.g. that the food supply of the predator population depends entirely on the prey population, and that during the process, the environment does not change in favor of one species and that genetic adaptation is sufficiently slow. Due to these assumptions, models might not perfectly reflect authentic biological systems where numerous factors interact simultaneously. Therefore, it is also important to conduct complimentary studies under natural conditions. This doctoral thesis aims to contribute to the understanding of the coexistence of ecologically similar species, by providing and analyzing empirical data on two sympatric mouse lemur species in Madagascar.

1.2 Biogeographic patterns in species

How species are geographically distributed throughout the world varies tremendously. The majority of the approximately two million different species of organisms so far described worldwide are found on land. A large number of species are found in species-rich areas such as the Amazon basin and in other tropical areas in Africa and southeast Asia (Cox & Moore 2000). Comparatively fewer species are found at higher latitudes (Stevens 1982). Some species have large geographic ranges while others are geographically restricted to a small local region. An example of a widely distributed species is the great spotted woodpecker (Dendrocopus major)

4 Chapter 1 General introduction whose range stretches over Europe (Mullarney et al. 1999). Its wide distribution contrasts largely to the range size of the subdesert mesite bird (Monias benschi), which is limited to an approximately 130 km long narrow coastal strip in the southwestern Madagascar (Sinclair & Langrand 2004). Factors determining how species arrange themselves spatially on a local scale as well on a larger geographic scale have been a major focus of research for decades. A number of factors have been shown to explain interspecific differences in geographic range size of species. The most significant are (1) local abundance, (2) body size, (3) climatic variability (“Rapoport‟s rule”), (4) biogeographic history, (5) ecological plasticity, and (6) competitive ability. A brief overview of these factors is hereby provided:

1.2.1 Local abundance The local abundance of species and range-size are positively correlated (anthropoid primates: Eeley & Lawes 1999, North American sucker and sunfishes: Pyron 1999, Finish stream insects: Heino 2005, birds: Bock 1984; Zuckerberg et al. 2009). Thus, locally abundant species are usually more widely distributed compared to locally rare species (review in Gaston et al. 2000). An example of a species that is locally abundant and widely distributed is the American crow (Corvus brachyrhynchos) inhabiting most of the northern America (Bock 1984). In contrast, the locally rare the white-headed woodpecker (Picoides albolarvatus) is geographically restricted to the pine-dominated montane forests from California to the Pacific northwest (Alexander & Burns 2006; Bock 1984). It has been proposed that species that are likely to attain larger local population sizes, possibly due to the ability to exploit a variety of resources, are also more likely to become more widespread than locally rare species (Brown 1984). High-density species may occupy a greater area due to a higher number of potential migrants, or simply by a higher probability for individuals to spread as a density-dependent effect (Gaston et al. 1997). Whether the positive relationship between local abundance and range size may also be a sampling artifact has been widely discussed. Detection may be more difficult in rare species since they are less likely to be sampled even though their actual distribution might be the same as that of a common species (Gaston & Blackburn 1997). However, the fact that a positive correlation between local abundance and range size is confirmed in well studied taxa such as breeding birds, implies that it is not merely a sampling artifact (Zuckerberg et al. 2009).

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1.2.2 Body size Range size can be either positively or negatively correlated with body size. Most studies show that small species tend to have small geographic ranges, whereas large species tend to be widely distributed (anthropoid primates: Eeley & Lawes 1999, African large mammals: Fernández & Vrba 2005, North American birds: Brown & Mauer 1987). This has been explained by a metabolic allometric effect: smaller-bodied animals (e.g. mice) generally have a higher metabolic rate relative to their body mass compared to larger-bodied species (e.g. elephants). Even though small animals require less overall food, they require more energy in relation to their smaller body mass (Blackburn & Gaston 1997). Consequently, smaller-bodied species may benefit by specializing on habitats that can provide a high quality diet (Mauer et al. 1992). Larger-bodied species, on the other hand, may survive on lower quality food. However, because of their larger size, they may be energetically constrained to have relatively large home ranges and low local population densities. Under these circumstances, only a large distribution may produce overall viable population sizes that are needed to prevent extinction (Brown 1981; Brown & Mauer 1987). For instance, forest fragmentation limits the distribution and the overall population of large species such as gorillas and chimpanzees, and is one of the main reasons why these species face a very high risk of extinction (Harcourt 2005). Another explanation for the positive correlation between body size and range size is that body size typically influences the competitive ability of a species. Larger species tend to have competitive advantages over smaller species (microtine rodents: Randall 1978, birds: Shelley et al. 2004; Travaini et al. 1998, fish. Blann & Healey 2006, primates: Peres 1996). Consequently, large species may be more successful during resource acquisition, translating into a higher potential for range expansion (this will be further discussed in the section “competitive ability”). Some studies also suggest a negative correlation between range size and body size (Glazier 1980). This negative correlation has, for instance, been explained by higher colonization ability in smaller species due to a higher reproductive rate (Lawton & Brown 1986). One example of how reproductive success might be linked to successful colonization is illustrated by three fern species in North America with differing abilities to self-fertilize. The most successful self-fertilizer was the species with the largest geographic range size, which was argued to be the consequence of a more effective colonization of new areas (Flinn 2006).

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1.2.3 Climatic variability (“Rapoport’s rule”) Species that live close to the equator tend to have relatively small geographic ranges, whereas species that occur further away from the equator tend to be more widely distributed. For instance, the range sizes of New World bats are smaller in the tropics and larger in temperate zones (Lyons & Willig 1997). The tendency for geographical range sizes to increase with increased distance from the equator is known as the “Rapoport‟s rule”. This phenomenon has been argued to result from the greater seasonal climatic variability in higher latitudes, favoring the selection of a broad climatic tolerance in species. High-latitude species should therefore be more plastic in their habitat choices compared to low-latitude species in the tropics, and should consequently be less spatially restricted in their dispersal options (Stevens 1989). Numerous studies showed that geographic range size increases with increasing distance from the equator (primates: Cowlishaw & Hacker 1997; Harcourt 2000, 2002; Eeley & Foleey 1999, mammals: Steven 1989; Fernández & Vrba 2005a). However, the empirical pattern is restricted to, or most distinct in the Palaearctic and Nearctic zone (above latitudes of 40-50°N) for many groups that follow this rule, suggesting that the “Rapoport‟s rule” may be a “local” phenomenon (Gaston et al. 1998; Rohde 1996).

1.2.4 Biogeographic history Historical biogeography describes how geological, climatic and ecological conditions in the past have influenced the current distribution of species (primates: Goodman & Ganzhorn 2004a, 2004b; Grubb 1982; Vences et al. 2009, mammals: Grubb 1982, birds: Diamond & Hamilton 1980, reptiles and amphibians: Araújo 2008). For instance, Grubb (1982) suggested that the dispersal of African mammals has been influenced by large historical climatic cycles during the Quaternary period. He suggested that a severe dry spell during this period resulted in a contraction of the forests in Africa down to three major areas, functioning as refugia for many species. During a subsequent moist climatic period mammals could disperse again following the pattern of forest expansion. The first severe dry period followed by a number of cycles of less severe drier periods and moist periods, was proposed to be most influential for the current distribution pattern of African mammals (Grubb 1982). In addition to large climatic changes in the past, ecological barriers (unfavorable vegetation) and physical barriers (rivers and mountains) could always have restricted the dispersal of species (Goodman & Ganzhorn 2004a)

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1.2.5 Ecological plasticity Generalist species with the ability to exploit a large variety of resources and habitats should be more widespread geographically compared to specialized species with narrower ecological niches (Brown 1984). A well-known example of a specialist that is also geographically restricted is the koala (Phascolarctos cinereus), whose diet consists almost entirely of eucalyptus leaves and whose range is limited to some regions in Australia. In contrast, the raccoon (Procyon lotor) is an example of a typical generalist with an omnivorous diet consisting of berries, insects, eggs and small animals etc., and whose natural range stretches throughout most of North and Central America (Wilson & Reeder 2005). The positive correlation between niche width and range size has been demonstrated in numerous studies (primates: Eeley & Foley 1999; Harcourt et al. 2002, mammals: Glazier 1980; Pagel et al. 1991, birds: Bock 1984; Brändle et al. 2002, fish: Pyron 1999, fleas: Krasnov et al. 2005, insects: Heino 2005; Komonen et al. 2004, temperate/boreal tree: Morin & Chuine 2006). However, it has also been argued that widespread species do not necessarily consist of generalists, but may instead be composed of several and differently specialized populations (Brown 1995; Harcourt et al. 2005; Stockwell & Peterson 2002). In this doctoral thesis, I will investigate whether the general predictions regarding ecological plasticity in species with differing geographic range sizes can be applied to two sympatric primate species.

1.2.6 Competitive ability If two species compete for the same resources, even a slight competitive advantage over another species can lead to reproductive advantages in the long term (Hardin 1960). One example of the occurrence of direct interspecific competition can be found in the sympatric microtine rodents Microtus montanus and M. longicaudus, where the comparatively stronger males of M. montanus gained better access to habitats preferred by both species (Randall 1978). Therefore, competitive ability might influence the survival and fitness of species on a local scale (Brown & Wilson 1956; Chase & Leibold 2003; Gause 1934; Hardin 1960), but might also influence their large- scale biogeography (Case et al. 2005; Cox & Moore 2000). A high competitive ability may be associated with both wide distribution as well as geographically restricted distribution of species. First, competitive ability could translate into a higher potential for range expansion. This may explain why widely distributed species have been able to expand geographically despite the presence of competing species (Darwin 1959; Brown

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1984; Hanski 1982; Holway 1999; Walck et al. 1999; Wilson & Keddy 1986). However, according to the proposed trade-off between competitive ability and dispersal/colonization (Levins & Culver 1971; Tilman et al. 1997), geographically restricted species are predicted to have a high competitive potential to allow them to maintain their often specialized ecological niches in the presence of widely distributed generalists (Miller 1967, mammals: Glazier & Eckert 2002; Hallett 1982). In this doctoral thesis, the role of interspecific competition in two ecologically similar species with a high potential to compete over resources will be explored.

1.3 Biogeographic rules in primates

The primate order has been estimated to contain 424 extant primate species, or 658 taxa when including subspecies (Rylands & Mittermeier 2009; Wilson & Reeder 2005). The majority of species are found in forest areas in the tropics in Central and South America, Africa, Madagascar and southern and eastern Asia (review in Lehman & Fleagle 2006). Various studies have investigated the biogeographic patterns in primates. As opposed to what has been observed in most taxa, there is no positive correlation between the local abundance of primates and their range size (Harcourt 2000, 2002). Instead, local population densities have been shown to decrease with increasing range size (Cowlishaw & Dunbar 2000, Harcourt et al. 2005). This pattern was, however, no longer apparent when the primates of Madagascar were excluded from the analysis (Cowlishaw & Dunbar 2000, Harcourt et al. 2005). The obvious influence of Madagascar and its lemuroids on various results of meta- analyses has been explained by the exceptional conditions in Madagascar. For instance, lemurs have exceptionally small average geographic range sizes (Mittermeier et al. 2010). They have only about one-tenth of the average range size of primates on the continent of Asia, where primates have the second smallest average geographic range size (Harcourt et al. 2002). Second, the “Rapoport‟s rule” seems to be only applicable to primates when Madagascar is excluded (Harcourt 2000). However, when primates of each continent were tested separately, Madagascar was the only continent where species closer to the equator tend to have smaller range sizes than species further away from the equator (Cowlishaw & Hacker 1997, Harcourt 2000). “Rapoport‟s rule” has also been shown to be applicable on lower taxonomic levels in primates.

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For instance, range sizes of both New World monkeys (Ruggiero 1994) and anthropoid primates in Africa increased with increasing distance from the equator (Eeley & Lawes 1999). As previously mentioned, the climatic variability hypothesis (Stevens 1989) implies that latitude and geographic range size also strongly correlates with niche width. Evidence shows that primate genera with small geographic ranges also tend to have narrow requirements for diet and habitat. For instance, the range size of African primates increases with climatic variability (Cowlishaw & Hacker 1997; Harcourt 2000), with increasing latitudes and habitat niche width (Eeley & Floley 1999; Fernández & Vrba 2005b; Harcourt 2002). Body size is another factor that is ambiguously correlated with geographical range size in primates. When the whole primate order was taken into account, no correlation was found between body size and range size (Harcourt et al. 2005). Furthermore, when continents were analyzed separately, no correlation was found except for the continent of America, where larger primates had larger ranges than smaller primates (Harcourt et al. 2005). However, on a lower taxonomic level, e.g. within the African anthropoids, larger species generally occurred over larger geographical areas, whereas small species were either widespread or relatively restricted in their ranges. In summary, no single factor can fully explain all variations in the biogeographic patterns of primates. Some biological trends can be applied to the entire primate order, while other trends only explain patterns observed in primates on one single continent, or in one taxonomic group. The individual history of a species also strongly influences biogeographic distribution patterns of a species (Harcourt et al. 2005). In general, species are on average younger and more ephemeral than deeper taxa such as genera, families or orders. Depending on the specific question, a suitable taxonomic level should be considered in order to answer the question (Harcourt et al. 2005). Harcourt et al. (2005) stated that failure to find any strong biological associations in a fairly well- studied clade such as primate, suggest several factors might be operating, perhaps different ones for different taxa. The aim of this doctoral thesis is to contribute to the field of biogeography by conducting complementary studies of two primate species under the exceptional conditions that is characteristic for Madagascar.

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1.4 The lemurs of Madagascar

Madagascar is the fourth largest island in the world. It is located about 400 km east of the coast of Mozambique (Figure 1-1). The 587,040 km2 large island was once part of the supercontinent Gondwana, but has been isolated for approximately 80-90 million years. The split of Gondwana started about 160 million years ago with Madagascar breaking off from the continent of Africa. The split continued with Madagascar breaking off from Antarctica at about 80-130 million years ago and then from India at about 80-90 million years ago (Scotese 2000; Yoder & Nowak 2006). The history of lemurs and their independent evolution in Madagascar started about 61 to 65 million years ago with the arrival of the first lemurs to the island (Roos et al. 2004; Yoder & Yang 2004). Although all lemurs originate from a common ancestor, interestingly the ancestral colonization of Madagascar probably took place millions of years after the island had already broken off from continental Africa (Scotese 2000; Yoder & Nowak 2006). The question on how ancestral lemurs crossed the 400 km wide Mozambique Channel to Madagascar has been extensively discussed, but is not yet completely solved (Kappeler 2000; Roos et al. 2004; Stankiewicz et al. 2005). Madagascar is known for its high primate diversity. About 100 endemic primate species, all belonging to the order Lemuriformes, are found here (Mittermeier et al. 2010). Lemurs are different from other primates in many aspects and typical characteristics for the lemur taxa include: a high proportion of nocturnal species (Mittermeier et al. 2010), the ability of some species to enter seasonal torpor during periods of low ambient temperatures and food shortage (Microcebus spp.: Atsalis 1999; Schmid & Ganzhorn 2009, Cheirogaleus spp.: Dausmann et al. 2004, 2005; Fietz & Ganzhorn 1999), reduced sexual dimorphism (Kappeler 1990) and female dominance (Pochron et al. 2003; Radespiel & Zimmermann 2001). Lemur communities are also characterized by a high local diversity of coexisting lemur species. For instance, up to 14 lemur species coexist in one forest (Ganzhorn et al. 1999; Rasolofoson et al. 2007). Lemurs are also distinguished by their exceptionally small average geographic range sizes. Their range sizes are only about one-tenth of the average range size of primates in Asia, where primates have the second smallest average geographic range size (Harcourt et al. 2002). Consequently, the restricted geographic distribution makes the majority of lemurs especially vulnerable for extinction: the 2008 IUCN Red List classifies 41% of the lemurs as threatened with extinction.

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Figure 1-1. Madagascar, marked in dark, is the fourth largest island in the world.

Extant lemurs can be divided into five families: the Cheiogaleidae (dwarf and mouse lemurs), the Daubentoniidae (Aye-Aye), the Lemuridae (lemurs), the Lepilemuridae (sportive lemurs) and the Indriidae: (wooly lemurs, sifakas and indri; Mittermeier et al. 2010). Since the first humans arrived on Madagascar approximately 2000 years ago, at least 17 lemur species of three families became extinct (Mittermeier et al. 2010). All extinct species belonged to genera

12 Chapter 1 General introduction larger than today‟s largest living lemur. The largest extinct lemur reached a body mass of approximately 200 kg (Godfrey & Jungers 2002), approximately 20 times the size of an indri (~9 kg) which is the largest extant lemur (Mittermeier et al. 2010). The smallest of all lemurs and also the smallest of all living primates are the mouse lemurs with a weight of 30 - 85 g (Rasoloarison et al. 2000).

1.5 Animal models: the gray mouse lemur (Microcebus murinus) and the golden-brown mouse lemur (M. ravelobensis)

In this doctoral thesis I use two mouse lemurs as primate models to investigate various mechanisms that might explain biogeographic patterns of lemurs in Madagascar. Mouse lemurs (Microcebus spp.) live in a wide range of forest habitats in Madagascar and are therefore a good model for understanding the distribution patterns of forest-dependent lemurs. The genus Microcebus is characterized by high species diversity. Eighteen mouse lemur species have so far been described (Mittermeier et al. 2010), inhabiting a variety of habitats including dry thorny scrub, lowland and highland humid forests as well dry deciduous forests (Mittermeier et al. 2010). With a body mass of 30 - 85 g and a head-to-tail length of less than 27 cm, these small lemurs are not much bigger than a mouse (Rasoloarison et al. 2000). Due to the often only slight phenotypic differences in size and color, different species of mouse lemurs cannot be easily distinguished from each other and are therefore so-called cryptic species (Olivieri et al. 2007). This study will focus on two congeners: the gray mouse lemur (M. murinus, Miller 1777; Figure 1-2) and the golden-brown mouse lemur (M. ravelobensis, Zimmermann et al. 1998; Figure 1-2). These two species show pronounced differences in geographic range size. M. murinus has the widest distribution of all mouse lemurs and ranges from the south to the northwest of the island, whereas M. ravelobensis occurs only in the area between the two large rivers, the Betsiboka and the Mahajamba in the northwest (Olivier et al. 2007; Figure 1-3). Their geographic ranges overlap in northwestern Madagascar where they are found in zones of both sympatry and allopatry (Rakotondravony & Radespiel 2009; Rendigs et al. 2003; Olivieri et al. 2007). In

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Figure 1-2. The gray mouse lemur (Microcebus. murinus) is shown to the left side and the golden-brown mouse lemur (M. ravelobensis) to the right side.

contrast to M. ravelobensis, M. murinus is found in sympatry with three other congeneric species throughout its wide range (M. berthae in the west: Dammhahn & Kappeler 2005, 2008; Schwab2000; Schwab & Ganzhorn 2004, M. myoxinus in the west: Louis et al. 2006; Yoder et al. 2000, and M. griseorufus in the southwest: Génin 2008; Rasoazanabary 2004; Yoder et al. 2002). Previous studies have revealed that the large difference in the distribution pattern of M. murinus and M. ravelobensis cannot be explained by variations in body size. The two species do not differ significantly in body length (M. 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). Moreover, neither interspecific variations in social system, nocturnal activity or seasonal reproduction have been able to explain their difference in range size. The social organization of both M. murinus and M. ravelobensis is a dispersed multi-male/multi-female system (Fietz 1999; Radespiel 2000; Weidt 2004). Both species are seasonal breeders (Schmelting et al. 2000), but female estrous is not as synchronized in golden-brown mouse lemurs as it is in gray mouse lemurs (Randrianambinina et al. 2003). Mouse lemur infants of both species are born at the beginning of the rainy season (Eberle & Kappeler 2006; Lutermann 2001; Quietzsch 2009). M. murinus as well as M. ravelobensis are solitary nocturnal foragers (Bearder 1987) but often sleep together in groups with other individuals during the day (Radespiel 2000; Weidt et al. 2004).

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Figure 1-3. The geographic range of M. murinus (marked in light gray) and the region where M. murinus and M. ravelobensis occur in sympatry (marked in dark gray) in Madagascar.

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M. murinus and M. ravelobensis show differences in their sleeping site ecology. For instance, M. murinus females usually sleep in stable groups of related females, whereas males usually sleep alone (Radespiel 2000; Radespiel et al. 1998, 2001). In contrast, M. ravelobensis forms sleeping groups comprising both sexes (Weidt et al. 2004). In addition M. murinus mainly uses tree holes for sleeping whereas M. ravelobensis mainly uses branches, lianas, leaves, and self-constructed spherical leaf nests (Radespiel et al. 2003; Thorén et al. 2009; Weidt 2001). The interspecific difference in sleeping site ecology has been linked to microhabitat differences in preferred forest structures (Rendigs et al. 2003). As long as lianas are available, possibly needed for shelter, M. ravelobensis shows a higher flexibility towards different forest microhabitat structures than its congener. In contrast M. murinus appears to be closely dependent on forest areas with trees containing tree holes for sleeping (Rendig et al. 2003). The interspecific difference in sleeping site ecology may reflect an ancient and divergent ecological niche differentiation that has allowed these two mouse lemur species to coexist by considerably interspecific competition (Radespiel et al. 2003). Whether these differences may also be the result of ongoing competition and a biased competitive potential is not yet known, and will be investigated in this doctoral thesis. The difference in microhabitat preferences cannot fully explain the regional distribution patterns and the coexistence of the two congeners in northwestern Madagascar. Further habitat differences (regional scale) revealed that M. ravelobensis inhabits a larger variety of habitats compared to M. murinus in this region. Whereas M. ravelobensis was found in dry habitats as well as in intermediate and humid areas in various population densities, M. murinus showed a preference for dry habitats (Rakotondravony & Radespiel 2009). Whether differences in feeding ecology can contribute to the understanding of the local coexistence of M. murinus and M. ravelobensis and their differences in distribution patterns is not yet known. However, in zones of extensive overlap, these ecologically similar species should show some degree of feeding niche differentiation. Both M. murinus and M. ravelobensis are known to have an omnivorous diet that includes gum, insect secretions, nectar, fruits, and animal matter (Joly & Zimmermann 2007; Radespiel et al. 2006). A preliminary study in the second half of the dry season suggested that the two species may differ in details of their diet composition. However, due to the limited time in which this study was conducted, seasonal dietary changes could not be investigated (Radespiel et al. 2006). Continuous data collection during an extended period of time accounting for seasonal changes in food availability that simultaneously

16 Chapter 1 General introduction investigates the feeding ecology of M. murinus and M. ravelobensis, was lacking until now. Therefore, this doctoral thesis aims to provide feeding data of these two species continuously collected during one year, to enable a comparative analysis of the feeding ecology of the two species.

1.6 Aim of study

The aim of this study is to investigate whether differences in food resource use and/or interspecific competition can contribute to the understanding of varying local abundance, coexistence as well as differences in geographic ranges sizes of the congeneric species M. murinus and M. ravelobensis in northwestern Madagascar. I will focus on the explanatory value of the plasticity in feeding resource use, feeding niche width and overlap, distribution and availability of key resources, as well as relative competitive potential of both species. I limited the study to females since food is assumed to be the most limiting resource for reproductive success for females, but not for males (Trivers 1972).

1.6.1 Resource use & characterization of feeding niches (Chapter 2) In chapter 1, I use data collected from one study site where both species occur in sympatry, to investigate whether the coexistence of M. murinus and M. ravelobensis is facilitated by reduced interspecific food competition resulting from feeding niche differentiation and/or reduced locomotor activity during periods of food shortage. The following questions are addressed:  How broad is the species-specific dietary regime (animals and plants) of the two mouse lemur species?  Are there species-specific specialisations concerning the consumed prey or plant species?  Are there species-specific differences concerning the relative proportion of different food items/species?  Are there seasonal dietary changes in the two congeners?  Are there species-specific differences in activity pattern of the two congeners?  Are there seasonal changes in activity pattern of the two congeners?  Do the two mouse lemurs reduce their locomotor activity during periods of food shortage, which may indicate an energy expenditure reduction?

17 Chapter 1 General introduction

1.6.2 Interspecific food competition (Chapter 3) In chapter 3, I use an experimental design to test whether the biogeographic patterns of the two sympatric mouse lemur species reflect differences in competitive potential. First, I investigate whether one species has a higher competitive potential, i.e. win more conflicts during encounter experiments, than the other species. Second, I investigate whether individuals with high competitive potential have priority of access to food and are less spatially restricted than individuals with low competitive potential. Third, I investigate whether one species consistently win more conflicts, has priority of access to food and is less spatially restricted than the other species. The following questions are addressed:  Are there interspecific interactions in the feeding context during caged experiments and if so, of what kind?  Are there any differences in body mass between dominant and subordinate individuals?  Do dominant individuals spend more time feeding compared to subordinate individuals?  Are dominant individuals less spatially restricted compared to subordinate individuals?  Does one species consistently win more conflicts than the other species?  Does the dominant species spend more time feeding compared to subordinate individuals?  Is the dominant species less spatially restricted compared to the subordinate species?

1.6.3 Distribution and availability of key resources (Chapter 4) In chapter 4, I use data collected from 21 study sites with varying densities of the two mouse lemurs, to investigate whether the widely distributed M. murinus is more plastic in its food resource use compared to the geographically restricted M. ravelobensis. Specifically, I investigate whether varying distribution of key food resources (estimated using botanical and observational data from three study sites) can explain the varying abundance of the two partially sympatric congeners (estimated using previously collected botanical, trapping and census data from 18 study sites). I expect that distribution and abundance of key food resources should play an more important role explaining the varying distribution patterns of the assumed generalist M. murinus than in the assumed specialist M. ravelobensis. The following questions are addressed:  Which food categories are consumed by the two congeners?  How large is the proportion of plant items consumed by the both species?  Which plant items are consumed?

18 Chapter 1 General introduction

 Which plant species are utilized by the two species?  Which are the potential key resources of the two species?  Which plant parts are consumed from the potential key resources?  How are these potential key resources distributed throughout the 18 study sites?  Can the varying abundance of potential key resources explain the varying abundance of M. murinus and M. ravelobensis in throughout the 18 study sites?

1.7 References

Alexander MP, Burns KJ. 2006. Intraspecific phylogeography and adaptive divergence in the white-headed woodpecker. The Condor 108:489-508. Amarasekare P. 2003. Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109-1122. Andriantompohavana RJR, Zaonarivelo SE, Engberg SE, Randriamampionona R, McGuire SM, Shore GD, Rakotonomenjanahary R, Brenneman RA, Louis jr EE. 2006. The mouse lemurs of northwestern Madagascar with a description of a new species at Lokobe Special Reserve. Occ Pap Tex Tech Univ Mus. 259:1–23. Araújo MB, Nogués Bravo D, Diniz Filho JAF, Haywood AM, Valdes PJ, Rahbek C. 2008. Quaternary climate changes explain diversity among reptiles and amphibians. Ecography 3:8-15. Atsalis S. 1999. Seasonal fluctuations in body fat and activity levels in a rain-forest species of mouse lemur, Microcebus rufus. Int J Primatol 20:883-910. Bearder SK. 1987. Lorises, bushbabies and tarsiers: diverse societies in solitary foragers. In: D Cheney, R Seyfarth, B Smuts, T Struhsaker, R Wrangham, editors. Primate Societies. University of Chicago Press, Chicago, p. 11–24. Bock CE. 1984. Geographical correlates of abundance vs. rarity in some North American winter landbirds. The Auk 101:266-273. Brändle M, Prinzing A, Pfeifer R, Brandl R. 2002. Dietary niche breadth for Central European birds: correlations with species-specific traits. Evol Ecol Res 4:643-657. Brown Jr WL, Wilson EO. 1956. Character displacement. Syst Zool 5:49-64.

19 Chapter 1 General introduction

Brown JH. 1981. Two decades of homage to Santa Rosalia: toward a general theory of diversity. Integrative Comp Biol 21:877. Brown JH. 1984. On the relationship between abundance and distribution of species. Am Nat 124:255-279. Brown JH, Maurer BA. 1987. Evolution of species assemblages: effects of energetic constraints and species dynamics on the diversification of the North American avifauna. Am Nat 130:1-17. Brown JH. 1995. Macroecology. Univ. Chicago Press, Chicago. 270 pp. Caughley G, Grice D, Barker R, Brown B. 1988. The edge of the range. J Anim Ecol 57:771-785 Ceballos G, Ehrlich PR. 2006. Global mammal distributions, biodiversity hotspots, and conservation. Proc Natl Acad Sci 103:19374-19379. Cowlishaw G, Hacker JE. 1997. Distribution, diversity, and latitude in African primates. Am Nat 150:505-512. Cowlishaw G, Dunbar R. 2000. Primate conservation biology: University of Chicago Press, 498 pp. Dammhahn M., Kappeler PM. 2005. Social system of Microcebus berthae, the world's smallest primate. Int J Primatol 26:407-435. Dammhahn M & Kappeler PM. 2008a. Small-scale coexistence of two mouse lemur species (Microcebus berthae and M, murinus) within a homogeneous competitive environment. Oecologia 157:473-483. Dammhahn M., Kappeler PM. 2008b. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29:1567-1589. Dausmann KH, Glos J, Ganzhorn JU, Heldmaier G. 2004. Hibernation in a tropical primate. Nature 429:825–826. Dausmann KH, Glos J, Ganzhorn JU, & Heldmaier, G. 2005. Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175: 147-155. Darwin C. 1859. On the origin of species by means of natural selection, or the preservation of

favoured races in the struggle for life. 1st edn. John Murray, London.

Diamond AW, Hamilton AC. 1980. The distribution of forest passerine birds and Quaternary climatic change in tropical Africa. J Zool Lond B 191:379-402.

20 Chapter 1 General introduction

Eberle M, Kappeler PM. 2006. Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus). Behav Ecol Sociobiol 60:582-588. Enquist BJ, Jordan MA, Brown JH. 1995. Connections between ecology, biogeography, and paleobiology: relationship between local abundance and geographic distribution in fossil and recent molluscs. Evol Ecol 96:586-604. Eeley HAC, Foley RA. 1999. Species richness, species range size and ecological specialisation among African primates: geographical patterns and conservation implications. Biodiversity and Conservation 8:1033-1056. Fernández MH, Vrba ES. 2005a. Body size, biomic specialization and range size of African large mammals. J Biogeogr 32:1243-1256. Fernández MH, Vrba ES. 2005b. Rapoport effect and biomic specialization in African mammals: revisiting the climatic variability hypothesis. J Biogeogr 32:903-918. Felsenstein J. 1985. Phylogenies and the Comparative Method. Am Nat 125:1-15. Fietz J. 1999. Mating system of Microcebus murinus. Am J Primatol 48:127–133. Fietz J, Ganzhorn JU. 1999. Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat? Oecologia 121:157-164. Flinn KM. 2006. Reproductive biology of three fern species may contribute to differential colonization success in post-agricultural forests. Am J Bot 93:1289. Ganzhorn JU, Wright PC, Ratsimbazafy J. 1999. Primate communities: Madagascar. In: JG Fleagle, C Janson, KE Reed, editors. Primate Communities. Cambridge: Cambridge University Press, p. 75–89. Gaston KJ, Blackburn TM, Spicer JI. 1998. Rapoport's rule: time for an epitaph? Trends Ecol Evol 13:70-74. Gaston KJ, TM Blackburn JJD, Greenwood RD, Gregory, R.M. Quinn, J.H. Lawton. 2000. Abundance-occupancy relationships. J Appl Ecol 37: 39–59. Gause GF. 1934. The struggle for existence. Williams & Wilkins, Baltimore, MD, 460 pp. Génin F. 2008. Life in unpredictable environments: first investigation of the Natural History of Microcebus griseorufus. Int J Primatol 29:303-321. Glazier DS. 1980. Ecological shifts and the evolution of geographically restricted species of North American Peromyscus (mice). J Biogeogr 7:63-83. Glazier DS, Eckert SE. 2002. Competitive ability, body size and geographical range size in small mammals. J Biogeogr 29:81-92

21 Chapter 1 General introduction

Godfrey LR, Jungers WL. 2002. Quaternary fossil lemurs. In: WC Harwig, editor. The primate fossil record, Cambridge University Press, Cambridge, p. 97-121. Goodman SM, O‟Connor S, Langrand O. 1993. A review of predation on lemurs: Implications for the evolution of social behavior in small, nocturnal primates. In: Kappeler PM, Ganzhorn JU, editors. Lemur social systems and their ecological basis. New York: Plenum Press, p. 51-66. Goodman SM, Ganzhorn JU. 2004a. Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers. J Biogeogr 31:47-55. Goodman SM, Ganzhorn JU. 2004b. Elevational ranges of lemurs in the humid forests of Madagascar. Int J Primatol 25:331-350. Grubb P. 1982. Refuges and dispersal in the speciation of African forest mammals. In: Prance GT, editor. Biological diversification in the tropics. Columbia University Press, New York, p. 537-53. Harcourt AH. 2000. Latitude and latitudinal extent: a global analysis of the Rapoport effect in a tropical mammalian taxon: primates. J Biogeogr 27:1169-1182. Harcourt AH, Coppeto SA, and Parks SA. 2002. Rarity, specialization and extinction in primates. J Biogeogr 29:445-456. Harcourt AH. An introductionary perspective: a gorilla conservation. 2003. In: AB Taylor, ML Goldmsmith, editors. Gorilla biology: a multidiciplinary perspective. Cambridge University Press, Cambridge (England), p. 407-413. Harcourt AH, Coppeto SA, and Parks SA. 2005. The distribution–abundance (density) relationship: its form and causes in a tropical mammal order, Primates. J Biogeogr 32:565-579. Hardin G. 1960. The competitive exclusion principle. Science 131:1292-1297. Harvey PH, Pagel MD. 1991. The comparative method in evolutionary biology: Oxford university press, Oxford, 239 pp. Heino J. 2005. Positive relationship between regional distribution and local abundance in stream insects: a consequence of niche breadth or niche position? Ecography 28:345-354. Holt RD, Keitt TH. 2005. Species‟ borders: a unifying theme in ecology. Oikos 108:3-6. Holway DA. 1999. Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecol 80:238-251. Hutchinson GE. 1957. Concluding remarks. Cold Springs Harbor Symp. Quant. Biol 22:415-427.

22 Chapter 1 General introduction

Joly M., Zimmermann E. 2007. First evidence for relocation of stationary food resources during foraging in a strepsirhine primate (Microcebus murinus). Am J Primatol 69:1045-1052. Kappeler PM. 1990. The evolution of sexual size dimorphism in prosimian primates. Am J Primatol 21:201-214. Kappeler PM. 2000. Lemur origins: rafting by groups of hibernators? Folia Primatol 71:422-425. Kappeler PM, Rasoloarison RM, Razafimanantsoa L, Walter L, and Roos C. 2005. Morphology, behaviour and molecular evolution of giant mouse lemurs (Mirza spp.) Gray, 1970, with description of a new species. Primate Report 71:3–26. Komonen A, Grapputo A, Kaitala V, Kotiaho JS, Päivinen J. 2004. The role of niche breadth, resource availability and range position on the life history of butterflies. Oikos 105:41-54. Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS. 2005. Host specificity and geographic range in haematophagous ectoparasites. Oikos 108:449-456. Lawton JH, Brown KC, Crawley MJ, Way MJ, Holdgate MW, May RM, Southwood R, O'Connor RJ. 1986. The Population and Community Ecology of Invading Insects (and Discussion). Philos T of the Roy Soc B 314:607-617. Levins R, Culver D. 1971. Regional coexistence of species and competition between rare species. Proc Natl Acad Sci 68:1246-1248. Louis Jr EE, Coles MS, Andriantompohavana R, Sommer JA, Engberg SE, Zaonarivelo JR, Mayor MI, Brenneman RA. 2006. Revision of the mouse lemurs (Microcebus) of eastern Madagascar. Int J Primatol 27:347-389. Louis Jr EE, Shannon J, Engberg E, McGuire S, McCormick M, Randriamampionona R, JFanaivoarisoa R, Bailey D, Mittermeier R, Rei L. 2008. Revision of the mouse lemurs, Microcebus (Primates, Lemuriformes), of Northern and Northwestern Madagascar with descriptions of two new species at Montagne D'Ambre National Park and Antafondro classified forest. The Journal of the IUCN/SSC Primate specialist Group No 23:19-38. Lyons SK, Willig MR. 1997. Latitudinal patterns of range size: methodological concerns and empirical evaluations for New World bats and marsupials. Oikos:568-580. Lutermann H. 2001. Weibchenassoziationen und Fortpflanzungsstrategien beim grauen Mausmaki (Microcebus murinus) in Nordwest-Madagaskar. Doctoral dissertation, University of Hannover. Mittermeier R, Louis E, Richardson M, Schwitzer C, Langrand O, Rylands B, Hawkins F,

23 Chapter 1 General introduction

Rajaobelina S, M R, C S, Langrand O, R, Ratsimbazafy J, Rasoloarison R, Roos C, Kappeler PM, Mackinnon PM. 2010. Lemurs of Madagascar. Panaamericana Formas e impresos S.A., Bogotá, Colombia: Conservation International. Morin X, Chuine I. 2006. Niche breadth, competitive strength and range size of tree species: a trade off based framework to understand species distribution. Ecol Lett 9:185-195. Mullarney K, Svensson L, Zetterström D, and Grant PJ. 1999. Collins bird guide: HarperCollins, London. Olivieri G, Zimmermann E, Randrianambinina B, Rasoloharijaona S, Rakotondravony D, Guschanski K, and Radespiel U. 2007. The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Mol Phylogenet Evol 43:309- 327. Pagel MD, May RM, Collie AR. 1991. Ecological aspects of the geographical distribution and diversity of mammalian species. Am Nat 137:791-815. Peterson AT. 1993. Adaptive geographical variation in bill shape of scrub jays (Aphelocoma coerulescens). Am Nat 142:508-527. Peterson AT, Varajas N. 1993. Ecological diversity in scrub jays, Aphelocoma coerulescens. In: TP Ramamoorthy, R Bye, A Lot, Fa J. Fa, J, editors. Biological diversity of Mexico: origins and distribution. Oxford University Press, New York, p. 309-317. Petter JJ. 1962. Ecological and behavioural studies of Madagascar lemurs in the field. Annals of the New York Academy of Sciences 102:267-281. Pither J. 2003. Climate tolerance and interspecific variation in geographic range size. Proc Roy Soc B 270:475. Pochron ST, Fitzgerald J, Gilbert CC, Lawrence D, Grgas M, Rakotonirina G, Ratsimbazafy R, Rakotosoa R, Wright PC. 2003. Patterns of female dominance in Propithecus diadema edwardsi of Ranomafana National Park, Madagascar. Am J Primatol 61:173-185. Porter LM. 2001. Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. Int J Primatol 22:961-992. Pyron M. 1999. Relationships between geographical range size, body size, local abundance, and habitat breadth in North American suckers and sunfishes. J Biogeogr 26:549-558. Quietzsch F. 2009. Zum Reproduktions- und Aufzuchtverhalten des Goldbrauner Mausmakis (Microcebus ravelobensis, Zimmermann et al. 1998). Doctoral dissertation, University of Veterinary Medicine Hannover.

24 Chapter 1 General introduction

Radespiel U. 1998. Die soziale Organisation des grauen Mausmakis (Microcebus murinus, J. F. Miller 1777) - eine Freilandökologische und laborexperimentelle Studie. Doctoral dissertation, University of Hannover Radespiel U. 2000. Sociality in the gray mouse lemur (Microcebus murinus) in northwestern Madagascar. Am J Primatol 51:21-40. Radespiel U, Ehresmann P, Zimmermann E. 2001. Contest versus scramble competition for mates: the composition and spatial structure of a population of gray mouse lemurs (Microcebus murinus) in north-west Madagascar. Primates 42: 207-220. Radespiel U, Zimmermann E. 2001. Female dominance in captive gray mouse lemurs (Microcebus murinus). Am J of Primatol 54:181-192. Radespiel U, Ehresmann P, Zimmermann E. 2003. Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in Northwestern Madagascar. Am J Primatol 59:139-151. Radespiel U. 2006. Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In L Gould, ML Sauther, editors. Lemur ecology and adaptation. New York: Springer, p. 211-233. Radespiel U, Olivieri G, Rasolofoson DW, Rakotondratsimba G, Rakotonirainy O, Rasoloharijaona S, Randrianambinina B, Ratsimbazafy JH, Ratelolahy F, Randriamboavonjy, Rasolofoharivelo T, Craul M, Rakotozafy L, Randrianarison RM. 2008. Exceptional Diversity of Mouse Lemurs (Microcebus spp.) in the Makira region with the description of one new species. Am J Primatol 70:1033-1046. Rakotondravony R, Radespiel U. 2009. Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. Am J Primatol 71:928-938. Rapoport EH. 1982. Aerography: Geographical strategies of species. Volume 1. 1st English ed. B. Drausal, translator. New York: Pergamon. Rasoloarison RM, Goodman SM, and Ganzhorn JU. 2000. Taxonomic Revision of Mouse Lemurs (Microcebus) in the Western Portions of Madagascar. Int J Primatol 21:963-1019. Rasolofoson D, Rakotondratsimba G, Rakotonirainy O, Rakotozafy L, Ratsimbazafy J, Rabetafika L, Randrianarison R. 2007. Influences des Pressions Anthropiques sur les Lé- muriens d‟Anantaka, dans la Partie Est du Plateau de Makira, Maroantsetra, Madagascar. Madagascar Conserv Develop 2:21-27.

25 Chapter 1 General introduction

Rasoazanabary E. 2004. A preliminary study of mouse lemurs in the Beza Mahafaly Special Reserve, southwest Madagascar. Lemur News 9:4-7. Rendigs A, Radespiel U, Wrogemann D, Zimmermann E. 2003. Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. Int J Primatol 24:47-64. Reimann WE. 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. Rohde K. 1996. Rapoport's rule is a local phenomenon and cannot explain latitudinal gradients in species diversity. Biodivers Lett 3:10-13. Roos C, Schmitz J, and Zischler H. 2004. Primate jumping genes elucidate strepsirrhine phylogeny. P Am Nat Acad Sci USA 101:10650-10654. Ruggiero A. 1994. Latitudinal correlates of the sizes of mammalian geographical ranges in South America. J Biogeogr 21:545-559. Rylands AB, Mittermeier RA. 2009. The diversity of the New World primates (Platyrrhini): an annotated taxonomy. In: PA Garber, A Estrada, JC Bicca-Marques, EW Heymann, KB Strier, editors. South American primates comparative perspectives in the study of behavior, ecology, and conservation. Springer, New York, p. 23-54. 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: Lourenço WR, Goodman SM, editors. Diversity and Endemism in Madagascar. Société de Biogéographie, Paris, p 165-75. Schmid J, Ganzhorn JU. 2009. Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften 96:737-741. Schoener TW. 1983. Field experiments on interspecific competition. Am Nat 122:240. Schwab D. 2000. A preliminary study of spatial distribution and mating system of pygmy mouse lemurs (Microcebus cf myoxinus). Am J Primatol 51:41-60. Schwab D, Ganzhorn JU. 2004. Distribution, population structure and habitat use of Microcebus berthae compared to those of other sympatric cheirogalids. Int J Primatol 25:307-330. Scotese CR. 2000. PALEOMAP Project: Earth History (paleogeographic maps). Dept Geol, Univ Texas, Arlington.

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Sinclair I, Langrand O. 2004. Birds of the Indian Ocean islands: Struik, p. 185. Stankiewicz J, Thiart C, Masters JC, and Wit MJ. 2006. Did lemurs have sweepstake tickets? An exploration of Simpson's model for the colonization of Madagascar by mammals. J Biogeogr 33:221-235. Stevens GC. 1989. The latitudinal gradient in geographical range: how so many species coexist in the tropics. Am Nat 133:240-256. Stockwell DRB, Peterson AT. 2002. Effects of sample size on accuracy of species distribution models. Ecol Model 148:1-13. Tavaré S, Marshall CR, Will O, Soligo C, Martin RD. 2002. Using the fossil record to estimate the age of the last common ancestor of extant primates. Nature 416:726-729. Townsend C, Harper J, Begon M. 2002. Ökologie. Berlin, Springer, 647 pp. Thorén S, Quietzsch F, Radespiel U. 2009. Leaf nest use and construction in the golden-brown mouse lemur (Microcebus ravelobensis) in the Ankarafantsika National Park. Am J Primatol 72:48-55. Tilman D, Lehman CL, Yin C. 1997. Habitat destruction, dispersal, and deterministic extinction in competitive communities. Am Nat 149:407-435. Trivers RL. 1972. Sexual selection and the descent of man. In: B. Campbell, editor. Parental investment and sexual selection. Aldine publishing company, Chicago, p. 136–179. Vieira EM, Port D. 2007. Niche overlap and resource partitioning between two sympatric fox species in southern Brazil. J Zool 272:57-63. Vences M, Wollenberg KC, Vieites DR, Lees DC. 2009. Madagascar as a model region of species diversification. Trends Ecol Evol 24:456-465. Walck JL, Baskin JM, Baskin CC. 1999. Relative competitive abilities and growth characteristics of a narrowly endemic and a geographically widespread Solidago species (Asteraceae). Am J Bot 86:820-828. Weidt A. 2001. Ökologie und Sozialbiologie von Weibchen des goldbraunen Mausmakis (Microcebus ravelobensis) während der Trockenzeit in Nordwest Madagaskar. Diploma thesis, University of Göttingen. Weidt A, Hagenah N, Randrianambinina B, Radespiel U, Zimmermann E. 2004. Social organization of the golden brown mouse lemur (Microcebus ravelobensis). Am J Phys Anthropol 123:40-51.

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Wilson DE, Reeder DM. 2005. Mammal species of the world, 3rd ed., vol. 2.Baltimore Johns Hopkins University Press, 2142 pp. Yoder AD, Burns MM, Génin F. 2002. Molecular evidence of reproductive isolation in sympatric sibling species of mouse lemurs. Int J Primatol 23:1335-1343. Yoder AD, Yang Z. 2004. Divergence dates for Malagasy lemurs estimated from multiple gene loci: geological and evolutionary context. Mol Ecol 13: 757-773. Yoder AD, Nowak MD. 2006. Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annu Rev Ecol Evol Syst 37:405. 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 Primatol 69:106-114. Zuckerberg, B., W.F. Porter, K. Corwin. 2009. The consistency and stability of abundance- occupancy relationships in large-scale population dynamics. J Anim Ecol 78: 172–181.

28

2

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

Published as: Thorén S, Quietzsch F, Schwochow D, Sehen L, Meusel C, Meares K, Radespiel U. 2011. International Journal of Primatology 32: 566-586.

29

2.1 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.

30

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Different competitive potential in two coexisting mouse

lemur species in northwestern Madagascar

Published as: Thorén S, Linnenbrink M, Radespiel U. 2011. International Journal of Physical Anthropology 145: 156-162.

31 Chapter 3 Competitive potential in two mouse lemur species

3.1 Abstract

Interspecific competition has been suggested to influence the biogeographic distribution patterns of species. A high competitive potential could entail species-specific advantages during resource acquisition that could translate into a higher potential for range expansion. We investigated whether differences in the competitive potential of the morphologically similar and partially sympatric gray mouse lemur (Microcebus murinus) and golden-brown mouse lemur (Microcebus ravelobensis) may help to explain differences in their geographic range sizes. We carried out encounter experiments with 14 pairs of captured female mouse lemurs of both species. The experimental dyads were tested in a two-cage arrangement, with individuals being separated from each other outside the experiments. Two days of habituation and four subsequent days of 1-h encounter experiments were conducted, before releasing the animals again in the wild. In general, the M. murinus individuals won significantly more conflicts than their partners. In eight of 14 tested pairs, there was a significant species bias in winning conflicts, and in 87.5% of these dyads, M. murinus was the „„dyad winner‟‟. A high competitive potential did not depend on body mass. Furthermore, „„dyad winners‟‟ spent more time feeding (P < 0.05) and were less spatially restricted than „„dyad losers‟‟ (P < 0.05). To conclude, our results suggest that the widely distributed M. murinus may indeed have a higher competitive potential than the regional endemic M. ravelobensis, which may, among other possible factors, have enabled this species to expand geographically, despite the presence of other competing congeners.

32

4

Can the distribution of key food plants explain the varying abundance of two mouse lemur species (Microcebus spp.) in northwestern Madagascar?

Submitted as: Thorén S, Sehen L, Rakotondravony R, Quietzsch F,

Radespiel U. American Journal of Primatology.

33 Chapter 4 Key food resources of two mouse lemur species

4.1 Abstract

Interspecific differences in resource use may explain varying geographic distribution of species. This study investigates whether interspecific differences in use of food resources and the varying distribution of these resources can explain the varying abundance M. murinus and M. ravelobensis in northwestern Madagascar. We identified potential key food plants for both species in three study sites and tested whether the distribution of these plants could explain the varying abundance of the two mouse lemur species in a set of 18 study sites. We identified key food plants by collecting feeding data from 17 female M. murinus and 18 female M. ravelobensis, and botanical data from nine plots and 36 transects. We identified eight and five potential key food plant species for M. murinus and M. ravelobensis, respectively. The presence of three of these food plants of M. murinus, but none of M. ravelobensis, could be linked to the varying abundance of these species in the 18 further sites. The two congeners utilized different items of their potential key plant species. Whereas M. ravelobensis consumed fruits exclusively, M. murinus consumed mainly gum, but also fruits and buds. The feeding strategy of M. murinus seems to be more adapted to drier habitats, whereas the feeding strategy of M. ravelobensis to more humid habitats. To conclude, interspecific differences in food resource use may explain the varying regional abundance and the coexistence of the two sympatric species, and might also explain their large-scale differences in geographic distribution patterns.

34 Chapter 4 Key food resources of two mouse lemur species

4.2 Introduction

Closely related species are likely to be ecologically similar due to a shared ancestry, and have therefore a high potential to compete over resources. Consequently, two competing species should show some degree of niche differentiation to stabily coexist in homogeneous and saturated environments (review in Amarasekare, 2003; Brown & Wilson 1956; Chase & Leibold 2003; Gause 1934; Hardin 1960). Niche differentiation can be achieved by resource partitioning (arthropods: Behmer & Joern 2008, invertebrates: Pianka 1973, birds: Garcia & Arroyo 2005, mammals: Azevedo et al. 2006; Sushma & Singh 2006). For example, resources that can be partitioned are space, water and sleeping sites, or food which is required for survival, growth and reproduction (Wedin & Tilman 1993, Korpimäki & Lagerström 1988, Ankney & MacInnes 1978). The availability and the spatial distribution of food resources may influence group size (Chapman et al. 1995), social system (Yamagiwa & Basabose 2009), foraging patterns of species (Corbin & Schmid 1995) as well as the geographic distribution pattern of species (Brown 1984; primates: Eeley & Foley 1999, Harcourt et al. 2002; mammals: Glazier 1980, Pagel et al. 1991; birds: Bock 1984, Brändle et al. 2002; fish: Pyron 1999; fleas: Krasnov et al. 2005; insects: Heino 2005, Komonen et al. 2004). Food resources that are believed to be particularly important are those available during the lean seasons when food is generally restricted, so called key resources (Marshall & Wrangham 2007). In this study we investigate whether the varying abundance and the coexistence of two partially sympatric mouse lemur species in northwestern Madagascar can be attributed to interspecific difference in the use of key food resource and the spatial distribution of those resources. We studied the ecologically and morphologically similar species, the widely distributed gray mouse lemur (Microcebus murinus) and the geographically restricted golden- brown mouse lemur (M. ravelobensis). These two species do not differ in basic aspects of their social organization, nocturnal activity, seasonal reproduction or body size. Both species live in a dispersed multi-male/multi-female system (Fietz 1999; Radespiel, 2000; Weidt et al. 2004), are seasonal breeders (Schmelting et al. 2000), are of similar body length and body mass (M. murinus: body mass = 83.3 ± 0.9mm; length = 53.9 ± 0.9g, M. ravelobensis: body mass = 81.3 ± 1.9g; length = 56.2 ± 1.8g; Zimmermann et al. 1998), and forage solitarily at night (Radespiel 2000; Schwab 2000; Weidt et al. 2004).

35 Chapter 4 Key food resources of two mouse lemur species

The two congeneric species show large differences in geographic range sizes. Whereas M. murinus inhabits the whole western part of Madagascar (Mittermeier et al. 2010), M. ravelobensis occurs only in northwest (Olivieri et al. 2007, Rakotondravony & Radespiel 2009, Rendigs et al. 2003, Zimmermann et al. 1998). In the region of their coexistence, in the dry deciduous forests of northwestern Madagascar, they occur in varying population densities and in zones of both sympatry and allopatry (Mester 2006, Rendigs et al. 2003, Rakotondravony & Radespiel 2009, Zimmermann et al. 1998). The varying abundance of the two species has partly been explained by differences in habitat preference (Rakotondravony & Radespiel 2009). Whereas M. ravelobensis was found in dry habitats as well as in intermediate and humid areas, M. murinus showed a significant preference for dry habitats (Rakotondravony & Radespiel 2009). However, it has not yet been addressed whether the varying abundance of the two mouse lemurs in northwestern Madagascar can be attributed to differences in feeding ecology. Both M. murinus and M. ravelobensis consume gum, insect secretions, nectar, fruits, and animal matter (Joly & Zimmermann 2007; Radespiel et al. 2006; Thorén et al. 2011). A previous study showed that despite a high dietary overlap of the two species, an interspecific feeding niche differentiation exists (Thorén et al. 2011). However, this previous study was limited to one site of coexistence of these species, and did not investigate whether differences in resource use also can explain their varying abundance throughout the region of geographic overlap in the northwest. Here we investigate whether the varying abundance of M. murinus and M. ravelobensis in northwestern Madagascar can be explained by the varying abundance of species-specific key resources. To investigate this we aim to (1) identify potential key plant species of M. murinus and of M. ravelobensis, (2) test whether the varying abundance of these potential key plants can explain the regional varying abundance of the two mouse lemur species.

4.3 Methods

4.3.1 Study sites We conducted the study during May to October 2003 & 2004, and between May 2007 and April 2008 (except for February 2008) in the dry deciduous forest in the Ankarafantsika National Park in northwestern Madagascar (135.000 ha), about 120 km southeast of Mahajanga. This region is 36 Chapter 4 Key food resources of two mouse lemur species 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 (Rakotondravony & Radespiel 2009). The strong seasonal climatic changes lead to yearly periods of food shortage (Rakotondravony & Radespiel 2009, Thorén et al. 2011). We collected data from a total of 21 different study sites, grouped by their joint access from nine different field camps (Figure 4-1). At three of these study sites (JBA, JBB, JBC), feeding and botanical data was collected to identify potential key plant species of M. murinus and M. ravelebensis. In JBA, M. murinus and M. ravelobensis were present in relatively equal abundance (52% individuals of M. murinus versus 48% individuals of M. ravelobensis), while M. murinus is predominately found in JBC (86% individuals of M. murinus versus 14% individuals of M. ravelobensis). In JBB (5.1 ha) M. ravelobensis is exclusively found (Rakotondravony and Radespiel 2009, Rendigs et al. 2003). JBA and JBB are easily accessible via grid system trails every 50 m, while the area of JBC (33.9 ha) was accessed via one central transect of ca. 1200 m length. At the other 18 study sites, population densities of M. murinus and M. ravelebensis, and the abundance of their potential key food plants were estimated. See underneath for further details.

4 2 JBC JBB JBA 1 3

Figure 4-1. Map of study in the Ankarafantsika National Park. Field camp: no. 1-10; study sites are indicated by their sites code and connected to respective field camp (for site codes, see Table 1 & 2).

37 Chapter 4 Key food resources of two mouse lemur species

4.3.2 Feeding data We collected feeding data in three study sites, locally known as JBA (16ο19´S, 46ο48´E, from May 2007 to April 2008), JBB (16ο15´S, 47ο02´E, from May 2007 to January 2008) and in Ankoririka, here referred to as JBC (16ο18´S, 46ο48´E, end of June to beginning of September 2007; Figure 4-1). In JBA (30.5 ha) and JBC (33.9 ha) the two species of mouse lemurs are found in sympatry. To obtain feeding data, we conducted focal observations of 16 female M. murinus (JBA: n =10, JBC: n=6) and 17 female M. ravelobensis (JBA: n=9, JBB: n=8) during 218 nights (18h00-23h00). We focused on females, since food is thought to be the most limiting resource for reproductive success of females, but not of males (Trivers 1972). Focal animals were trapped (using Sherman traps) and equipped with radio collars (3g, TW4-button cell tags, Biotrack, UK). We located the females using a telemetry receiver with an antenna (TR-4 with RA-14K antenna; Telonics Inc, Mesa, AZ) and a headlamp (Petzl Myo5 or Petzl tikka plus, France). We used a flashlight (Mag-Lite® 3D-Cell, USA), a dictaphone (Olympus digital voice recorder, WS- 320M, Japan) and a GPS device (Garmin GPS 60 or Garmin etrex vista, USA) to facilitate nightly observations. The observer-animal distance varied from 1 to 15 m. We recorded all feeding bouts (defined as feeding episodes of continuous feeding, with less than 20 seconds interruptions). We categorized the feeding bouts by plant items (gum, buds, fruits or leaves) and non-plant items (arthropods, reptiles or insect secretions). We classified the feeding trees taxonomically. In total we identified the food items of 783 feeding bouts (M. murinus: JBA=255; JBB=101, M. ravelobensis: JBA=126, JBB=301). We were able to identify plant species for a total of 422 plant feeding bouts (54%), 236 of which were of M. murinus and 186 were of M. ravelobensis.

4.3.3 Botanical data To estimate the abundance of consumed plant species in JBA, JBB and JBC, we installed vegetation plots (30m x 30m) and transects (50m long) at each study site. We inventoried a total of nine plots (JBA: 4, JBB: 3, JBC: 2), and 36 transects (JBA: 18, JBB: 9, JBC: 9). All individual plants within the vegetation plots and all individual plants within a 2-m strip on both sides of the 50m transects were determined to species level whenever possible. 96.9% of all specimens in the plots (n = 8907) in JBA, 97.1% (n = 4248) in JBB, and 99.2% (n = 4902) in JBC could be so determined (for further details, see Sehen et al. 2010). We did not inventory lianas. To investigate the seasonal availability of specific plant items consumed (leaves, buds and fruits), we collected

38 Chapter 4 Key food resources of two mouse lemur species plant phenology data along four transects (total length ≈ 320m) located in the study area. We included 577 individual plants (JBA: 272, JBB: 183, JBC: 120), which we marked and identified taxonomically (lianas, shrubs, and trees, belonging to 125 genera). About twice monthly, we monitored the abundance of flowers, leaves and fruits (including both fleshy and non-fleshy fruits), estimated as the percentage of the total capacity of each individual plant. In JBA and JBB we determined plant phenology during the complete year, while data collection in JBC was restricted to the months of June, mid-August and mid-September. We lack data in JBA and JBB for mid-August, for the beginning of September 2007, for January, February, and for the beginning of March 2008. In addition, we lack plant phenology data for JBB in mid-July, mid- December, mid-March, and mid-April. To complement our own collected data, we used plant phenology data collected during the years 2001 and 2002 (Reimann 2002).

4.3.4 Identification of potential key resources Three main criteria needed to be fulfilled for a plant species to be categorized as a potential key feeding plants of M. murinus or M. ravelobensis: (1) Usage frequency of plant species: We considered plant species to be potentially important when at least 3 feeding bouts had been recorded for this plant, and it had been consumed by a minimum of two individuals of a species, (2) Usage during the dry season: We considered only those feeding plants as potentially important that were consumed or seasonally available during the dry season, (3) Relative abundance of the feeding plants at the three different study sites: Feeding plants were considered to be potential key resources of M. murinus it they were present in high abundance in JBA and JBC (with high relative abundance of M. murinus) and in low abundance or absent in JBB. We considered feeding plants to be potential key resources for M. ravelobensis when available in high abundance in JBB (with high relative abundance of M. ravelobensis) and in lower abundances or absent in JBA and JBC. Unfortunately, we lack abundance data for lianas in the botanical plots and transects. In addition, for two consumed tree species (Dalbergia tsiandalana & Vatambotrika), we lack botanical data at the species level. To minimize the risk that we excluded important food plants due to the lack of data, we considered the plant species with lacking abundance data as potential key resources when they fulfilled criteria 1 & 2. Thus, the liana Acacia schweinfurthii, consumed by M. murinus, and Dichapetalum leucosia consumed by M. ravelobensis, were included as potential key food plants, despite the lack of density data.

39 Chapter 4 Key food resources of two mouse lemur species

4.3.5 Linkage between key resources, presence and abundance of mouse lemurs In order to investigate the relationship between potential key resources and the varying abundance of the two mouse lemur species in northwestern Madagascar, we used botanical and capture data from 18 different study sites throughout the Ankarafantsika National Park (Figure 4- 1). Data collection took place between May 2003 and October 2004, along 1000m transects at all sites. Mouse lemurs were trapped during 3-4 nights per site, using about 100 Sherman live traps per capture night. The abundance of plant species was estimated using the point-centered quarter (PCQ) method (Mueller-Dombois & Ellenberg 1974). Every 40 m along the trails at each study site, a circular plot (radius of 10 m) was sampled (26-28 plots per site). The circular plot was divided into four quarters. In each quarter, we sampled four plants that belonged to one of four vegetation categories and were the closest representatives of that category to the center point. We sampled the following vegetation categories: (1) Trees with a diameter in breast height (DBH) between 2.0 and 4.9 cm, (2) Trees with a DBH between 5.0 and 9.9 cm, (3) Trees with a DBH ≥ 10 cm (4) shrub with a height ≥ 1 m. Thus, in every PCQ-plot, we sampled a total of up to 16 individual plants. In total we sampled 5120 individual plants in the eighteen study sites (mean: 282±22.3 plants per site). We used multiple regression analyses (p < 0.05) in order to test whether the varying abundance of mouse lemurs trapped at each of the 18 study sites could be linked to the abundance of potential key food plants (STATISTICA 6, StatSoft, Inc. 2004). We used two different ways to estimate and analyze the relationship between the abundance of the two mouse lemur species and the abundance of the potential key plant species: (1) relationship between the absolute number of captured mouse lemurs per species and the absolute number of specimen of the sampled key plant species per site, and (2) relationship between the number of individual mouse lemurs per hectare (taken from Rakotondravony & Radespiel 2009) and the relative proportion of each key plant species among all sampled plants per site.

4.4 Results

4.4.1 Potential key feeding plants The diet of female M. murinus and female M. ravelobensis consisted of gum, fruits, buds, insect secretions and arthropods. In addition, female M. ravelobensis consumed leaves and reptiles 40 Chapter 4 Key food resources of two mouse lemur species

(Figure 2). A large proportion of their diet consisted of plant items (M. murinus: JBA = 86.3%, JBC = 20.8%; M. ravelobensis: JBA = 54.0%, JBB = 58.5%). M. murinus consumed plant items from 19 different plant species (Table 4-1) and M. ravelobensis from 31 plant species (Table 4- 2). On the basis of the defined criteria, eight of the 19 feeding plants of M. murinus (Acacia schweinfurthii, Astrotrichilia asterotricha, Baudouinia fluggeiformis, Dalbergia tsiandalana, Mystroxylum aethiopicum, Noronhia boinensis, Rhopalocarpus similis and Rothmania reniformis), and five of the 31 food plant species of M. ravelobensis (Dichapetalum leucosia, qualified as potential key resources. From half of the eight plant species of M. murinus, two different plant parts were consumed, such as gum and fruits, or fruits and buds. From 75.0% of the potential key foods of M. murinus, gum was consumed. In contrast, the plant items consumed from all five potential key plant species of M. ravelobensis were fruit.

Figure 4-2. Relative proportion (%) of food items consumed by M. murinus and M. ravelobensis during the study, separated by study site; FB, number of feeding bouts, n, number of females. Grangeria porosa, Malleastrum gracile, Monanthotaxis pilosa and Psychotria obtusifolia)

41 Chapter 4 Key food resources of two mouse lemur species

Table 4-1. Plant species consumed by M. murinus. Descriptive data are given regarding plant items consumed, number of feeding bouts (FB), number of different individuals (IND), whether consumed or available during the dry season, and the relative abundance of the feeding plants at the three different study sites (less: relatively low abundance, more: relatively high abundance). Fulfilled criteria are marked in bold. Plant species that fulfilled the criteria defined as key plant species are marked in grey.

Plant species Plant item FB IND Dry season Site availability

1 Acacia schweinfurthii gum 8 5 yes Liana 2 Astrotrichilia asterotricha gum 9 4 yes JBA, JBB (less) & JBC 3 Baudouinia fluggeiformis fruit, gum 31 2 yes JBA & JBC (less) 4 Bussea perrieri gum 1 1 yes JBA & JBC 5 Cedrelopsis microfoliolata gum 1 1 yes JBA & JBC 6 Commiphora sp gum 1 1 yes JBA, JBB (less) & JBC 7 Crateva simplicifolia fruit 1 1 yes JBA 8 Dalbergia tsiandalana fruit, gum 30 3 yes Missing data 9 Mammea punctata buds 5 2 yes JBA, JBB & JBC (less) 10 Mystroxylum aethiopicum gum 18 5 yes JBA & JBC 11 Noronhia boinensis fruit 13 2 yes JBA, JBB (less) & JBC 12 Poupartia sylvatica gum 3 1 yes JBA 13 Rhopalocarpus similis fruit, gum 96 12 yes JBA, JBB (less) & JBC 14 Rothmania reniformis bud, fruit 10 2 yes JBA, JBB (less) & JBC

15 Sakayala fruit 2 1 no liana

16 Scolopia inappendiculata gum 1 1 yes JBA, JBB (less) & JBC

17 Strychnos madagascariensis fruit 1 1 no JBA, JBB (more) & JBC

18 Vahimboay gum 2 1 yes liana

19 Vitex sp fruit 3 1 yes JBA, JBB (less) & JBC

4.4.2 Relationship between potential key resources, presence and relative abundance of mouse lemurs The number of mouse lemurs captured at each of the 18 different study sites varied per species from 0-30 individuals (M. murinus: 0-25, M. ravelobensis: 0-30; Table 4-3 & 4-4). The two mouse lemur species were found in sympatry in eight sites (Ambanjakely I, Ambanjakely III, Andofombobe I, Andoharano II, Ankoririka II, Antanimbary, Bevazaha II, Beronono II). In three sites only M. murinus was found (Ambodimanga, Andofombobe II, Andoharano III), while M. ravelobensis was found alone in seven sites (Ambanjakely II, Ampatika, Andofombobe III, Andoharano I, Ankoririka I, Beronono I, Bevazaha I).

42 Chapter 4 Key food resources of two mouse lemur species

Table 4-2. Plant species consumed by M. ravelobensis; Descriptive data are given regarding plant items consumed, number of feeding bouts (FB), number of different individuals (IND), whether consumed or available during the dry season, and the relative abundance of the feeding plants at the three different study sites (less: relatively low abundance, more: relatively high abundance). Fulfilled criteria are marked in bold. Plant species that fulfilled the criteria defined as key plant species are marked in grey. Plant species Plant item FB IND Dry season Site availability 1 Anacolosa pervilleana fruit 1 1 no JBA (more), JBB & JBC 2 Alibiza gummifera gum 1 1 yes JBB & JBC 3 Antidisma petiolare fruit 4 2 no JBB 4 Astrotrichilia asterotricha fruit, gum 3 1 yes JBA, JBB (less) & JBC 5 Bridelia pervilleana fruit 6 1 yes JBB & JBC 6 Baudouinia fluggeiformis gum 8 1 yes JBA & JBC 7 Canthium sp fruit 6 3 yes JBB (less) & JBC 8 Cinnamosma fragrans gum 10 1 yes JBA (less) & JBC 9 Dichapetalum leucosia fruit 28 4 yes liana 10 Erythroxylum platycerum fruit 1 1 no JBB & JBC (less) 11 Grangeria porosa fruit 6 2 yes JBA, JBB (more) & JBC 12 Grewia sp fruit 2 1 yes JBB 13 Grewia radula fruit 4 1 no JBB 14 Landolphia myrtifolia fruit 1 1 yes liana 15 Malleastrum gracile fruit 4 3 yes JBA (less) & JBB 16 Molinaea retusa fruit 1 1 yes JBA , JBB (more) & JBC 17 Monanthotaxis pilosa fruit 9 3 yes JBB 18 Noronhia boinensis fruit, leaves 2 1 yes JBA, JBB (less) & JBC 19 Poupartia sylvatica gum 10 2 yes JBA 20 Psychotria obtusifolia fruit 9 2 yes JBB 21 Rhopalocarpus similis gum 15 5 yes JBA, JBB (less) & JBC 22 Rothmania reniformis fruit, gum 9 2 yes JBA, JBB (less) & JBC 23 Scolopia inappendiculata fruit, gum 9 3 yes JBA, JBB (less) & JBC 24 Strychnos madagascariensis fruit 2 2 no JBA, JBB (more) & JBC 25 Securinega capuronii gum 5 1 yes JBA & JBC 26 Tectonia grandis bud 1 1 yes JBB 27 Vahimaintso fruit 1 1 no liana 28 Vahimavo bud, fruit 7 1 no liana 29 Vahimboay fruit 11 1 no liana 30 Vatambotrika fruit 1 1 no missing data 31 Vahamraju flower, fruit 9 3 no liana

43 Chapter 4 Key food resources of two mouse lemur species

The potential key resource of M. murinus, Dalbergia tsiandalana was excluded from the data set due to lacking data: the genus was sampled, but information about species level was missing. Due to its rareness, Acacia schweinfurthii was excluded as potential key resource of M. murinus: it was only found in one of the eighteen study sites, and was never sampled in sites with presence of M. murinus. The total number of sampled trees of the remaining six potential key plant species of M. murinus varied from zero to 36 specimens per site. These six plant species were sampled at 18.2% (Mystroxylum aethiopicum) to 90.9% (Rothmania reniformis) of the study sites where M. murinus was found (mean: 53.0%±26.0), and in 0 (Astrotrichilia asterotricha, Mystroxylum aethiopicum, Noronhia boinensis) to 71.4% (Rhopalocarpus similis) of the study sites where M. murinus was not found (mean: 23.8%±29.5). The probability to find M. murinus given the presence of the six potential key food plant species varied between 61.5 and 100%. Three of the species consumed by M. murinus, Astrotrichilia asterotricha, Mystroxylon aethiopiopicum and Noronhia boinensis were only found in study sites with presence of M. murinus. Whenever at least one of these three plant species was present, individuals of M. murinus were captured. The multiple regression analyses revealed that the absolute number of captured individuals of M. murinus was significantly correlated with the absolute number of tree specimen of the potential key resources (R² = 0.89, p = 0.00009). Three of the four plant species Astrotrichilia asterotricha (B = 1.57±0.46, β = 0.35; = p = 0.006), Baudouinia fluggeiformis (B = 1.70±0.37, β = 0.50; p = 0.001) and Noronhia boinensis (B = 0.47±0.09, β = 0.67, p = 0.0005) contributed significantly to the overall correlation. On the other hand, Mystroxylum aethiopicum (B = -1.20±1.12, β = -0.13, p = 0.31), Rhopalocarpus similis (B = 0.20±0.11, β = 0.18, p = 0.10) and Rothmania reniformis (B = -0.45±0.39, β = -0.12, p = 0.28) did not contribute significantly. The multiple regression between the population density of M. murinus and the percentage of the potential key resources among all sampled trees did not reveal any significant correlation (R² = 0.44, p = 0.33; Astrotrichilia asterotricha: B = 0.38±0.68, β = 0.13, p = 0.60, Baudouinia fluggeiformis: B = 0.23±0.68, β = -0.09, p = 0.74, Mystroxylum aethiopicum: B = -0.20±1.73, β = -0.03, p = 0.91, Noronhia boinensis: B = 0.28±0.15, β = 0.60, p = 0.10, Rhopalocarpus similis: B = 0.15±0.16, β = 0.23, p = 0.36, Rothmania reniformis: B = 0.06±0.53, β = -0.03, p = 0.91)

44 Chapter 4 Key food resources of two mouse lemur species

Table 4-3. Descriptive data for seven of the eight potential key plant species of M. murinus. For each site, the abundance of M. murinus is given both as the total number of captured individuals and as individuals per hectare (M. mur ind./ha); the abundance of each plant species is given as the absolute number of sampled trees per species (#) and their relative proportion among all sampled trees of all plant species (AA: Astrotrichilia asterotricha MA: Mystroxylon aethiopiopicum, BF: Baudouinia fluggeiformis, NB: Noronhia boinensis, RS: Rhopalocarpus similis, RR: Rothmania reniformis). Data are lacking for: Dalbergia tsiandalana; Camp: field camp, FC: field code; sites with absence of M. murinus are white-marked, whereas sites with presence of M. murinus are grey-marked.

Camp Study site FC # M. mur # AS # AA # BF # MA # NB # RS # RR M. mur/ha % AS % AA % BF % MA % NB % RS % RR 8 Ambanjakely II ABK2 0 2 0 0.7 6 Ampatika APK 0 1 12 7 0 0.4 4.9 2.9 9 Andofombobe III ABE3 0 1 2 4 0 0.3 0.7 1.4 7 Andoharano I ANO1 0 4 3 0 1.5 1.1 2 Ankoririka I AKR1 0 0 5 Beronono I BER1 0 1 16 0 0.4 5.7 4 Bevazaha I BEV1 0 0 7 Andoharano II ANO2 1 3 2 0.29 1.1 0.7 6 Antanimbary ATB 4 2 1 4 4 0.74 0.7 0.4 1.5 1.5 2 Ankoririka II AKR2 4 1.76 5 Beronono II BER2 5 22 1 2.23 7.3 0.3 3 Ambodimanga AGA 6 6 3 2 3 missing 2.3 1.2 0.8 1.2 8 Ambanjakely I ABK1 7 2 19 2 2.84 0.8 7.3 0.8 8 Ambanjakely III ABK3 8 6 2 0.86 2.2 0.7 9 Andofombobe II ABE2 11 2 2 14 4 4 5.28 0.7 0.7 5.0 1.4 1.4 9 Andofombobe I ABE1 13 3 3 28 8 1 0.99 1.0 1.0 9.5 2.7 0.3 7 Andoharano III ANO3 21 3 7 7 1 1.67 1.1 2.5 2.5 0.4 4 Bevazaha II BEV2 25 4 36 8 3 4.76 1.3 11.9 2.6 1.0 Probability to find M. murinus: 0% 100% 75.0% 100% 100% 61.5% 76.9%

45 Chapter 4 Key food resources of two mouse lemur species

Table 4-4. Descriptive data for two of the five potential key plant species of M. ravelobensis. For each site, the abundance of M. ravelobensis is given both as the total number of captured individuals and as individuals per hectare (M. rav ind./ha); the abundance of each plant species is given as the absolute number of sampled trees per species (#) and their relative proportion among all sampled trees of all plant species (GP: Grangeria porosa, MG: Malleastrum gracile). Data are lacking for Dichapetalum leucosia, Monanthotaxis pilosa & Psychotria obtusifolia; Camp: field camp, FC: field code, sites with absence of M. ravelobensis are white-marked, whereas sites with presence of M. ravelobensis are grey-marked. Camp Study site FC M. rav # GP # MG # M. rav ind/ha GP % MG % 3 Ambodimanga AGA 0 1 0.0 0.4 9 Andofombobe II ABE2 0 5 0.0 1.8 7 Andoharano III ANO3 0 0.0 9 Andofombobe I ABE1 1 0.1 9 Andofombobe III ABE3 1 28 1 2.4 9.8 0.3 6 Antanimbary ATB 2 14 0.4 5.1 4 Bevazaha II BEV2 2 2 0.4 0.7 6 Ampatika APK 6 5 1.5 2.1 8 Ambanjakely I ABK1 6 7 2.4 2.7 8 Ambanjakely III ABK3 6 15 0.6 5.5 5 Beronono II BER2 9 12 4 4.0 4.0 1.3 2 Ankoririka II AKR2 10 1 4.4 0.3 7 Andoharano II ANO2 12 3.5 5 Beronono I BER1 12 11 25 9.4 3.9 9.0 8 Ambanjakely II ABK2 15 34 missing 12.6 7 Andoharano I ANO1 22 6.7 4 Bevazaha I BEV1 22 19 9 2.6 5.9 2.8 2 Ankoririka I AKR1 30 72 8.3 23.7 Probability to find M. ravelobensis: 83.3% 100%

Distribution data for three of five potential key plant species of M. ravelobensis were lacking. Since the 2003/04 data set contained only the genus information for these taxa (Dichapetalum leucosia, Monanthotaxis pilosa and Psychotria obtusifolia) they could not be included in following analysis. The fact that Psychotria obtusifolia and Monanthotaxis pilosa were never observed in JBB, suggests that these species are indeed rare and possibly do not explain the varying abundance of M. ravelobensis in the sites of northwestern Madagascar. Distribution data, however, were available for Grangeria porosa and Malleastrum gracile. The total number of sampled trees of these two species varied from zero to 72 specimens per site. Grangeria porosa was as equally often sampled in sites with absence of M. ravelobensis as in sites with presence of M. ravelobensis (66.7% of the sites). Malleastrum gracile was only found

46 Chapter 4 Key food resources of two mouse lemur species in the study sites with presence M. ravelobensis (40.0% of the sites). The probability to find M. ravelobensis given the presence of the two potential key food plant species varied between 83.3 and 100%. The multiple regression revealed that the total captured individuals of M. ravelobensis was not significantly correlated with total number of trees of the two potential key resources (R² = 0.65, p = 0.21; Grangeria porosa: B = -0.14±0.38, β = -0.15, p = 0.74, Malleastrum gracile: B = 0.27±0.15, β = 0.72, p = 0.17). The multiple regression between the density of M. ravelobensis and the relative proportion of Grangeria porosa and Malleastrum gracile in the botanical sample did also not reveal any significant correlation (R² = 0.61, p = 0.25; Grangeria porosa: B = - 0.19±0.34, β = -0.24, p = 0.61, Malleastrum gracile: B = 0.21±0.14, β = -0.63, p = 0.23).

4.5 Discussion

4.5.1 Do mouse lemurs possess key food plants? Interspecific differences in resource use may contribute to the understanding of how species coexist locally, but may also explain large differences in geographic distribution patterns of coexisting species (Brown 1984). We studied two sympatric congeneric species, the widely distributed M. murinus and the locally restricted M. ravelobensis, that partially coexist in the dry deciduous forests in northwestern Madagascar. We investigated whether interspecific differences in their use of key food plant species and the varying distribution of these resources can explain the varying regional distribution patterns of the two mouse lemur species. Our results show that key plant species and their distribution seem to explain the regional distribution pattern of the widely distributed M. murinus, but probably not that of the geographically restricted and locally abundant M. ravelobensis. The varying abundances of three of the eight potential key plant species of M. murinus (Astrotrichilia asterotricha, Baudouinia fluggeiformis, Noronhia boinensis) were positively correlated with the varying abundance of M. murinus at 18 different study sites. The absence/presence of these three plant species did not fully explain the absence/presence of M. murinus, but when any of these resources were present, the probability to find this mouse lemur species was high (75-100%). We did not find a significant relationship between the abundance of M. murinus and its potential key resources when we used population densities of M. murinus and the relative abundance of each plant species. Since the two mouse 47 Chapter 4 Key food resources of two mouse lemur species lemur species were indistinguishable during the nightly census, the density of each species was calculated based on their relative representation in the total number captured mouse lemurs. Thus, the density of one species depended on how many individuals of the other species were captured and this calculation procedure may therefore have influenced the results. Furthermore, the relative proportion of potential key plant species among all sampled trees is influenced by the number of suitable trees within a plot that belonged to any of the four defined vegetation categories and may not necessarily be a good measurement of varying abundance. Consequently, the absolute number of mouse lemurs and plant species may be a more accurate estimate of their varying abundance at the 18 study sites. In contrast to what we found in M. murinus, the varying abundance of M. ravelobensis could neither be linked to the presence nor to the varying abundance of the five potential key food plants. Widely distributed species are typically widespread due to the ability to exploit a large variety of resources (primates: Eeley & Foley 1999, Harcourt et al. 2002; mammals: Glazier 1980, Pagel et al. 1991; birds: Bock 1984, Brändle et al. 2002; fish: Pyron 1999; fleas: Krasnov et al. 2005; insects: Heino 2005, Komonen et al. 2004). In contrast, our data indicate that the widely distributed M. murinus, but not the locally distributed M. ravelobensis relied on certain key plant species. The lack of correlation between the abundance of certain food resources and the varying abundance of M. ravelobensis indicates that this species may not be highly specialized with regard to food plant species. In this study we focused on key plant species. It is possible that the distribution of the two mouse lemur species and especially that of M. ravelobensis may be better explained by abundance of specific plant items. The two congeners utilized different parts of their potential key plant species. M. ravelobensis only consumed fruits from these plant species. In contrast, M. murinus showed a wider use of its potential key plant species and often (50%) consumed more than one food item from these. The food items consumed by M. murinus were fruits and buds as well as gum, which is a food resource thought to be especially important in environments where fruiting is irregular (Génin 2004). This higher food item plasticity and strong reliance on gum in M. murinus may explain its successful establishment in dryer habitat types (Rakotondravony & Radespiel 2009). High-quality food resources such as fruits rather than low-quality fallback foods have previously been suggested to be important determinants of distribution pattern (Doran-Sheehy et al. 2009), and may have influenced the distribution pattern of M. ravelobensis. The fruit bias in M. ravelobensis was not only observed among the potential key plant species, but was also

48 Chapter 4 Key food resources of two mouse lemur species observed when including all plant species that were extensively used during the year and available during the lean season. Since, fruits are only seasonally available, it is possible that M. ravelobensis cannot afford to rely on certain key plant species, but might have to use those plant species with the available fruits. Consequently, M. ravelobensis may rely on more humid habitats where the fruit availability is generally higher, which may explain why this species is also found in higher abundances in intermediate and humid dry habitats in comparison to the dry habitats preferred by M. murinus (Rakotondravony & Radespiel 2009). It is also possible that other food resources than plant items are of importance for the spatial distribution of M. murinus and M. ravelobensis. A previous study (Thorén et al. 2011) suggested that in particular M. ravelobensis consumed a considerable proportion of insect secretions. The abundance of stationary insect colonies, producing the sugary secretion, was already shown to influence the ranging behavior of gray mouse lemurs in western Madagascar (Corbin & Schmid 1995), and might also be of importance for M. ravelobensis in northwestern Madagascar.

4.5.2 What other factors might influence the varying abundance of M. murinus and M. ravelobensis in northwestern Madagascar? In addition to food, other resources might also have influenced the distribution pattern of M. murinus and M. ravelobensis. For instance, the two species show interspecific differences in sleeping site ecology. M. murinus mostly sleeps in tree holes, whereas M. ravelobensis is more often found in dense vegetation or in self-constructed leaf nests (Radespiel et al. 2003, Thorén et al. 2009). Available tree holes have been proposed to be a limiting resource for female M. murinus (Lutermann et al. 2010, Rendig et al. 2003). In contrast, M. ravelobensis seems to show a higher flexibility with regard to different forest microhabitats than its congener as long as there are lianas which they often use as shelter (Rendig et al. 2003). These interspecific differences in sleeping site requirements might partly explain the species-specific habitat preferences (Rakotondravony & Radespiel 2009). It is also possible that other factors than resources limit the geographic distribution of species. For instance, interspecific competition should be prominent in closely related species (Hardin, 1960), and could have implications for species survival and stability of species communities (Brown & Wilson 1956, Brown et al. 1996, Chase and Leibold, 2003, Gause, 1934; Glazier & Eckert 2002, Hanski & Gyllenberg 1997). A high competitive potential in M. murinus

49 Chapter 4 Key food resources of two mouse lemur species was previously suggested to restrict the distribution pattern of another sympatric, but much smaller congeneric species (M. berthae) in western Madagascar (Dammhahn & Kappeler 2008, Schwab & Ganzhorn, 2004). An elevated competitive potential in M. murinus compared to M. ravelobensis was also suggested by another study (Thorén et al. in press), and may explain that the widely distributed M. murinus has been able to expand geographically despite the presence of other competing species. However, the spatial restriction of M. murinus to a limited number of sites in northwestern Madagascar implies that other factors than its competitive potential over its congener might determine its regional distribution pattern, and the identified key food plants may be involved in this regulation on the regional level.

4.5.3 Conclusions The use of key plant species and their varying distribution seem to have influenced the regional distribution pattern of M. murinus, but probably not that of M. ravelobensis. In contrast, the abundance of M. ravelobensis may rather depend on the availability of fruits. Alternatively or in addition, the relatively high insect secretion consumption of M. ravelobensis (Thorén et al. 2011), suggests that the availability of homopteran larvae may also explain the varying abundance of M. ravelobensis. Our findings provide support for interspecific differences in key resource use between the two partially sympatric species M. murinus and M. ravelobensis. The feeding strategy of M. murinus seems to be more adapted to drier habitats, whereas the feeding strategy of M. ravelobensis to more humid habitats. The interspecific differences in food resource use may explain the varying regional abundance and the coexistence of the two sympatric species, and might also explain their large-scale differences in geographic distribution patterns.

4.6 Acknowledgements

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 the permission to work in the Ankarafantsika National Park. We also want to thank the local staff of the National Park for their continuous support. We are grateful to Blanchard Randrianambinina and Solofo Rasoloharijaona for their valuable help during the study. Many thanks go to Kate Meares, Doreen Schwochow,

50 Chapter 4 Key food resources of two mouse lemur species

Sonja Kunath, Pièrre Razafindraibe, Fanomezantsoa Rakotonirina and Roger Randrimparany for their enthusiastic help during data collection. We are also thankful to Roger Edmont for botanical expertise. All field handling and sampling procedures accorded 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.

4.7 References

Ankney CD, MacInnes CD. 1978. Nutrient reserves and reproductive performance of female lesser snow geese. The Auk 95:459-471. Bock CE. 1984. Geographical correlates of abundance vs. rarity in some North American winter landbirds. The Auk: 101:266-273. Brändle M, Prinzing A, Pfeifer R, Brandl R. 2002. Dietary niche breadth for Central European birds: correlations with species-specific traits. Evol Ecol Res 4:643-657. Brown JH. 1984. On the relationship between abundance and distribution of species. Am Nat 124:255-279. Brown JH. 1995. Macroecology. Univ. Chicago Press, Chicago, 270 pp. Brown JH, Stevens GC, Kaufman DM. 1996. The geographic range: size, shape, boundaries, and internal structure. Annu Rev Ecol System 27:597-623. Brown Jr WL, Wilson EO. 1956. Character displacement. Systematic Zool 5:49-64. Chase JM, Leibold MA. 2003. Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago, 216 pp. Corbin GD, Schmid J. 1995. Insect Secretions Determine Habitat Use Patterns by a Female Lesser Mouse Lemur (Microcebus murinus). Am J Primatol 37:317-324. Dammhahn M, Kappeler PM. 2008. Small-scale coexistence of two mouse lemur species (Microcebus berthae and M, murinus) within a homogeneous competitive environment. Oecologia 157:473-483. Doran Sheehy D, Mongo P, Lodwick J, Conklin Brittain NL. 2009. Male and female western gorilla diet: Preferred foods, use of fallback resources, and implications for ape versus old world monkey foraging strategies. Am J Phys Anthropol 140:727-738. 51 Chapter 4 Key food resources of two mouse lemur species

Eeley HAC, Foley RA. 1999. Species richness, species range size and ecological specialisation among African primates: geographical patterns and conservation implications. Biodivers Conserv 8:1033-1056. Glazier DS. 1980. Ecological shifts and the evolution of geographically restricted species of North American Peromyscus (mice). J Biogeogr 7:63-83. Glazier DS, Eckert SE. 2002. Competitive ability, body size and geographical range size in small mammals. J Biogeogr 29:81-92. Hanski I, Gyllenberg M. 1997. Uniting two general patterns in the distribution of species. Science 275:397-400. Harcourt AH, Coppeto SA, Parks SA. 2002. Rarity, specialization and extinction in primates. J Biogeography 29:445-456. Heino J. 2005. Positive relationship between regional distribution and local abundance in stream insects: a consequence of niche breadth or niche position? Ecography 28:345-354. Komonen A, Grapputo A, Kaitala V, Kotiaho JS, Päivinen J. 2004. The role of niche breadth, resource availability and range position on the life history of butterflies. Oikos 105:41-54. Korpimäki E, Lagerström M. 1988. Survival and natal dispersal of fledglings of Tengmalm's owl in relation to fluctuating food conditions and hatching date. J Anim Ecol 57:433-441. Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS. 2005. Host specificity and geographic range in haematophagous ectoparasites. Oikos 108:449-456. Lalandy S, Goetze D, Rajeriarison C, Roger E, Thorén S, Radespiel U. 2010. Stuctural and floristic traits of habitats with differing relative abundance of the lemurs Microcebus murinus and M. ravelobensis in northwestern Madagscar. Ecotropica 16:15-30. Lutermann H, Verburgt L, Rendigs A. 2010. Resting and nesting in a small mammal: sleeping sites as a limiting resource for female grey mouse lemurs. Anim Behav 79:1211-1219. Marshall AJ, Wrangham RW. 2007. Evolutionary Consequences of Fallback Foods. Int J of Primatol 28:1219-1235. Mester, S. 2006. Populationsdynamik nachtaktiver Kleinlemuren (Microcebus murinus und M. ravelobensis) in Nordwest-Madagaskar. Doctoral dissertation. University of Veterinary Medicine, Hannover, Germany.

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Mittermeier R, Louis E, Richardson M, Schwitzer C, Langrand O, Rylands B, Hawkins F, Rajaobelina S, M R, C S, Langrand O, R, Ratsimbazafy J, Rasoloarison R, Roos C, Kappeler PM, Mackinnon PM. 2010. Lemurs of Madagascar. Panaamericana Formas e impresos S.A., Bogotá, Colombia: Conservation International. Mueller-Dombois D, Ellenberg H. 1974. Aims and methods of vegetation ecology, New York, 547 pp. Olivieri G, Zimmermann E, Randrianambinina B, Rasoloharijaona S, Rakotondravony D, Guschanski K, Radespiel U. 2007. The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Molecular Phylogenet Evol 43:309- 327. Pagel MD, May RM, Collie AR. 1991. Ecological aspects of the geographical distribution and diversity of mammalian species. Am Nat 137:791-815. Pyron M. 1999. Relationships between geographical range size, body size, local abundance, and habitat breadth in North American suckers and sunfishes. J Biogeogr 26:549-558. Radespiel U, Ehresmann P, Zimmermann E. 2003. Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in Northwestern Madagascar. Am J Primatol 59:139-151. Rakotondravony R, Radespiel U. 2009. Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. Am J Primatol 71:928-938. Reimann W. 2002 Koexistenz und Nahrungsökologie von Weibchen des grauen und goldbraunen Mausmakis (Microcebus murinus und M. ravelobensis) in Nordwest-Madagaskar, Unpublished dissertation, School of Veterinary Medicine Hannover, Hannover, Germany. Rendigs A, Radespiel U, Wrogemann D, Zimmermann E. 2003. Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. Int J Primatol 24:47-64. Schwab D, Ganzhorn JU. 2004. Distribution, population structure and habitat use of Microcebus berthae compared to those of other sympatric cheirogalids. Int J Primatol 25:307-330. Thorén S, Quietzsch F, Radespiel U. 2009. Leaf nest use and construction in the golden-brown mouse lemur (Microcebus ravelobensis) in the Ankarafantsika National Park. Am J Primatol 72:48-55.

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Thorén S, Quietzsch F, Schwochow D, Sehen L, Meusel C, Meares K, Radespiel U. 2011. 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. Int J Primatol, DOI: 10.1007/s10764-010- 9488-1. Thorén S, Linnenbrink M, Radespiel U. In press. Different competitive potential in two coexisting mouse lemur species in northwestern Madagascar. A J Phys Anthropol. Trivers RL. 1972. Sexual selection and the descent of man. In: B. Campbell, editor. Parental investment and sexual selection. Aldine publishing company, Chicago, p 136–179. Wedin D, Tilman D. 1993. Competition among grasses along a nitrogen gradient: initial conditions and mechanisms of competition. Ecol Monogr 63:199-229. Yamagiwa J, Basabose AK. 2009. Fallback foods and dietary partitioning among Pan and Gorilla. Am J Physl Anthropol 140:739-750. 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 Primatol 69:106-114.

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5

General discussion

55 Chapter 5 General discussion

The three chapters included in this doctoral thesis aimed to investigate whether differentiated food resource use (Chapters 2 & 4) and interspecific competition (Chapter 3) of M. murinus and M. ravelobensis in northwestern Madagascar could explain (1) their coexistence, (2) their varying regional abundance, and (3) their pronounced difference in geographic range size. In this chapter, I will summarize the main results and discuss them from an evolutionary perspective.

5.1 Resource use (Chapter 2 & 4)

5.1.1 Implications for coexistence For species to stably coexist, they should show some degree of niche differentiation to avoid or reduce interspecific competition for essential resources (review in Amarasekare 2003; Brown & Wilson 1956; Chase & Leibold 2003; Gause 1934; Hardin 1960). Chapters 2 & 4 provide evidence for the existence of feeding niche differentiation between the sympatric species M. murinus and M. ravelobensis. As it has been shown in other sets of sympatric species (arthropods: Behmer & Joern 2008, invertebrates: Pianka 1973, birds: Garcia & Arroyo 2005, mammals: Azevedo et al. 2006; Sushma & Singh 2006), chapter 2 revealed signs of food partitioning between M. murinus and M. ravelobensis. A previous study of three sympatric primate species in Bolivia showed that coexisting species utilized the same set of food resources but to a different degree (Porter 2001). This was also shown in this study: the dietary regimes of M. murinus and M. ravelobensis overlapped. However, during two of the four seasonal periods, some jointly used food items (insect secretions, fruits and/or arthropods) were consumed to different extents. M. ravelobensis consumed proportionally more insect secretions and fewer arthropods than M. murinus during the late dry season, and consumed proportionally more insect secretions and less fruits than M. murinus during the early rainy season. Additionally, M. ravelobensis also consumed leaves, whereas M. murinus consumed buds exclusively. The high consumption of insect secretions in M. ravelobensis suggests that this food resource is of particular importance for this species. A high consumption of insect secretions also characterizes the diet of M. berthae, the sympatric congener of M. murinus in western Madagascar (Dammhahn & Kappeler 2008b). Additional dietary differences were revealed in the plant species consumed. M. murinus and M. ravelobensis used a considerable proportion of their food plant species exclusively,

56 Chapter 5 General discussion

resulting in only partially overlapping diets. Differentiated feeding niches of coexisting species are expected to be especially important during periods of food shortage in order to avoid competition over limited food resources (Hladik et al. 1980). However, the dietary overlap of M. murinus and M. ravelobensis was surprisingly high during the early part of the dry season (48.5%). The high overlap may be due to higher food abundance than expected during this period, which was also the proposed explanation for the lacking niche separation in diet composition between three sympatric Cheirogaleus species in Mandena (Lahann 2007). The regular presence of seeds in mouse lemur feces in the early, but not in the late dry season, supports that fruit abundance during this period was still relatively high. High dietary overlap in the early dry season also coincided with a period of reduced locomotor activity in M. murinus, expressed as increased resting (median of 72.3% during P1 compared to 17.9-20.9% during P2-P4) that coincided with decreased foraging (median: 0.0%) and feeding (median: 5.3%) activities. This reduced locomotor activity was not observed in M. ravelobensis. In contrast, this species spent its yearly lowest time resting during this period (median: 17.4%). M. murinus spent approximately one third of the resting time inside tree trunks. This species is known to enter torpor during periods of low ambient temperatures and food shortage (Schmid 1999, 2000; Schmid & Ganzhorn 2009), which may reduce energetic costs considerably (Kobbe & Dausmann 2009; Schmid & Kappeler 2005; Schülke & Ostner 2007). Minimized energetic requirements have previously been suggested to reduce competition over food resources. For instance, in western Madagascar, C. medius hibernates up to 7 months a year during the dry season, which might help to explain its coexistence with the much smaller M. murinus and M. berthae (Dausmann et al. 2005). Whether M. murinus entered torpor inside the tree trunks could not be determined. Nevertheless, if an animal rests, it does not spend much energy on locomotion. Therefore, the reduced activity of M. murinus may indicate reduced energy expenditure, which may also lead to reduced feeding competition with M. ravelobensis. Consequently, it is possible that this reduced feeding competition during this period allowed the dietary overlap to be relatively high. To summarize this section, the coexistence of M. murinus and M. ravelobensis appears to be facilitated by a combination of interspecific feeding niche differentiation and reduced competition over available food resources during lean seasons due to reduced energetic requirements in M. murinus.

57 Chapter 5 General discussion

5.1.2 Implications for varying regional abundance & geographic range size Chapters 2 & 4 investigated whether differentiated food resource use of M. murinus and M. ravelobensis can explain their varying regional abundance and their difference in geographic range size. It has been proposed that species having the ability to exploit a variety of resources are likely to attain larger local abundances and are more likely to become more widespread than locally rare species (Brown 1984). Thus, generalists should be locally abundant and more widespread geographically compared to specialized species (Brown 1984). In contrast to this prediction, the geographically restricted M. ravelobensis is locally more abundant species in northwest Madagascar relative to the widely distributed M. murinus (Rakotondravony & Radespiel 2009). Various studies have shown a positive correlation between niche width and geographic range size (primates: Eeley & Foley 1999; Harcourt et al. 2002, mammals: Glazier 1980; Pagel et al. 1991, birds: Bock 1984; Brändle et al. 2002, fish: Pyron 1999, insects: Heino 2005; Komonen et al. 2004; Krasnov et al. 2005, temperate/boreal tree: Morin & Chuine 2006). This positive correlation was also observed in M. murinus and its sympatric congener M. berthae in western Madagascar (Dammhahn & Kappeler 2008a; 2008b; 2010). In contrast to these studies, the results in this doctoral thesis suggest that the geographically restricted M. ravelobensis had the broader feeding niche over the widely distributed M. murinus in northwestern Madagascar. This was indicated by the larger variety of food items consumed by M. ravelobensis compared to M. murinus. Whereas both species consumed tree gum, insect secretions, fruits, buds and arthropods, M. ravelobensis also consumed leaves and reptiles. Furthermore, M. ravelobensis utilized a larger variety of plant species compared to the M. murinus (31 compared to 19). Thus, an ability to exploit a larger variety of food resources cannot explain the larger geographic range of M. murinus, but might explain how M. ravelobensis has been able to attain large local population sizes in northwestern Madagascar. In general, M. ravelobensis occurs in relatively low densities in dry habitats compared to their high densities in more humid habitats. In contrast, M. murinus was found in relatively low densities in intermediate habitats while being mostly absent in humid habitats (Rakotondravony & Radespiel 2009). In chapter 4, it was investigated whether varying abundance of the two mouse lemurs in northwestern Madagascar could be explained by differences in key food plants and the varying abundance of these plant species. Key resources (referred to here as those food resources available during the lean season when food is generally restricted) should be

58 Chapter 5 General discussion particularly important for the behavior and the ecology of species (Marshall & Wrangham 2007). It was suggested that key plant species and their distribution help to explain the regional distribution pattern of the widely distributed M. murinus, but not that of the geographically restricted and locally abundant M. ravelobensis. In M. murinus, the abundance of three plant species (Astrotrichilia asterotricha, Baudouinia fluggeiformis, Noronhia boinensis) out of eight proposed key food plant resources was positively correlated with the abundance of the mouse lemurs at 18 different study sites. However, the absence/presence of these three resources did not fully explain the absence/presence of M. murinus, but when any of these resources were present, the probability to find M. murinus was high (75-100%). The lack of correlation between the abundance of certain food resources and the varying abundance of M. ravelobensis indicates that this species may not be highly specialized with regard to food plant species. The spatial distribution of the two mouse lemur species could also be influenced by the abundance of certain key plant items and not necessarily by specific plant species. There was an interspecific difference in what parts were consumed from the potential key resources of M. murinus and M. ravelobensis. M. murinus showed a wider use of its potential key resources by consuming several different parts from each plant species, in contrast to M. ravelobensis that only consumed fruits from its potential key resources. It is possible that a more opportunistic use of food items has allowed M. murinus to become ecologically and geographically more plastic. A more opportunistic use of food items in M. murinus compared to its congener was already suggested by its seasonally influenced diet (northwestern Madagascar: chapter 2, western Madagascar; Dammhahn & Kappeler 2008b). In addition, M. murinus consumed gum very frequently, which is a food item that should be especially important in environments where fruiting is irregular (Génin 2004). In contrast, the potential key plant species provided only fruits for M. ravelobensis. The fruit bias in M. ravelobensis was also observed when including all plant species and not only potential key plants (their varying abundance was not linked to the varying abundance of the mouse lemurs). Fruits were extensively used over the year and seemed to have been available also during the lean season. M. ravelobensis consumed fruits from 10 of the 12 plant species which were fed on during the dry season, which emphasizes the importance of fruits for this species. Since fruits of specific plant species are only seasonally available, it is possible that M. ravelobensis cannot afford to rely only on certain key fruit plant species, but might have to be rather opportunistic with regard to the use of available fruits. In contrast, the opportunistic use of various plant items and the high proportion of gum in the diet of M. murinus indicate that

59 Chapter 5 General discussion this species may have a feeding strategy that is more adapted to drier habitats, whereas M. ravelobensis might rely more on humid habitats where the fruit availability is generally higher. A dry-adapted resource use might also explain why M. murinus is rare in the northwestern Madagascar. This region constitutes the northern edge of the range of M. murinus and may contain less suitable habitats, which could explain the low local abundance of this species. Throughout its range, M. murinus is found in a range of different habitats types including lowland tropical dry forest, sub-arid thorn scrub, gallery forest, spiny forest and secondary forest (review Radespiel 2006). All of these habitats can be considered to be relatively dry. Thus, the large geographic range of M. murinus might not require a broad niche. Instead, an adaptation to dry habitats might have allowed M. murinus to expand spatially into regions with drier climates. In contrast, resource use strategies adapted to more humid habitats in M. ravelobensis might explain its higher densities in more humid habitats, but may also explain the why the distribution of this species is restricted to the lowland areas in northwestern Madagascar. It is important to consider that other food resources than plants may also help to explain the varying abundance of M. ravelobensis. The diet of M. ravelobensis also consisted of arthropods and insect secretion. However, as indicated from fecal analyses in chapter 2, the arthropod consumption in M. ravelobensis was lower than that of M. murinus during the lean period of the year (the second half of the dry season). Consequently, increased significance of arthropods in the diet of M. ravelobensis compared M. murinus is not likely to explain the differences in local abundance of the two species. However, insect secretion that has previously been shown to influence the ranging behavior in mouse lemurs in western Madagascar (Corbin & Schmid 1995) was a particularly important food resource for M. ravelobensis during the second half of the dry season. The proportion of insect secretions of the total diet of M. ravelobensis was shown to be higher in a study site with high density of this species (JBB, median: 71.4% ±53.0) compared to a site with lower density (JBA, median: 37.5±53.0; Thorén, unpublished data), which indicate that insect secretion may have influenced the varying abundance of M. ravelobensis. This will be investigated further in future studies. To summarize this section, consistent with observations of other Malagasy primates (Harcourt et al. 2005), the pronounced differences in geographic range size could not be explained by differences in feeding niche width. Furthermore, M. murinus was not as generalistic as predicted from its large geographic range size, and M. ravelobensis was not as specialized as predicted from its restricted range size. These types of findings have evoked the question of

60 Chapter 5 General discussion whether widespread taxa are really generalist, or whether they rather consist of several differently specialized populations (Brown 1995, Harcourt et al. 2005). Whether this is the case in M. murinus is not yet known. Nevertheless, the results from this doctoral thesis suggest an adaptation to drier habitats in M. murinus compared to an adaptation to more humid habitats in M. ravelobensis. Thus, two species with different geographic ranges do not necessarily need to show different degrees in their ability to exploit resources. Instead, both mouse lemur species might be rather specialized, but may differ in range size due to a varying availability of suitable and species-specific habitats.

5.2 Interspecific food competition (Chapter 3)

Interspecific competition occurs frequently within species communities (review in Schoener, 1983), and should be particularly high between congeneric species due to ecological homologies of closely related species (Harvey & Pagel 1991). The outcome of repeated agonistic interactions between sympatric species is often consistent and stable, with one species having a higher competitive potential than the other (Rowley & Christian 1976; Shelley et al. 2004; Traviani et al 1998). Chapter 3 investigated the relative competitive potential of two ecologically similar species with a high potential to compete over resources. It could be shown that M. murinus has a higher competitive ability than M. ravelobensis in standardized encounter experiments. In the majority of the total conflicts, M. murinus was the winner over M. ravelobensis. Furthermore, in the majority of the dyads where one species won significantly more conflicts than the other, M. murinus was the winner. A high competitive potential should result in increased success when exploiting preferred resources and consequently better fitness in the dominant species (Bernstein 1981; Kaufmann 1983; Magnuson et al. 1979). Consistent with this, a high competitive potential in this study was positively associated with a longer feeding time. In addition, dominant individuals spent more time in the cage of their partner compared to the subordinate individuals, which may indicate that individuals with relatively high competitive potential were less spatially restricted by the presence of their partner than vice versa. Despite the bias in competitive potential, M. murinus was not completely dominant over M. ravelobensis. Instead, conflicts could in principle be won

61 Chapter 5 General discussion by both species. It is, however, enough that one species has even a slight advantage over another species for this species to dominate in the long term (Hardin 1960).

5.2.1 Implications for coexistence Under natural conditions, competitive advantages like that of M. murinus over M. ravelobensis, could lead to advantages during food acquisition. In contrast, species with low competitive potential may suffer from high energetic costs when ensuring access to preferred resources. If the energetic costs of coexistence are be sufficiently high, the subordinate species should either be replaced or should shift its ecological niche in order to avoid further competition (Abramsky et al. 2001; Kotler et al. 1993; Randall 1978; Sandlin 2000; Ziv et al. 1993). For instance, two sympatric species in Uganda, the blue monkey (Cercopithecus mitis) and the red-tailed monkey (C. ascanius) utilize the same food resources. While the dominant species C. mitis is typically able to aggressively defend food resources, the competitively weaker C. ascanius seems to survive by feeding on the low fruit density left behind by C. mitis (Houle et al. 2006). Another example was observed in competing hummingbirds, where two competitive subordinate species changed their foraging strategy in the presence of a comparatively dominant species (Sandlin, 2000). The difference in competitive potential between the two mouse lemur species in this study might explain the observed feeding niche differentiation of M. murinus and M. ravelobensis in zones of sympatry. In zones of competition, competitively subordinate species are usually forced to occupy a niche (realized niche) that is narrower than the full range of environmental conditions under which it can exist (fundamental niche; Hutchinson 1957). Chapter 2 & 4 report that even though M. ravelobensis generally utilized a larger variety of plant species compared to the M. murinus (31 compared to 19), this was not the case in the zone of extensive overlap with M. murinus (JBA, 18 different identified plant species compared to 12). It is possible that the lower competitive potential of M. ravelobensis has forced this species to utilize a smaller realized niche in this area. However, it is also possible that the site of sympatry did not contain the preferred feeding plant species of M. ravelobensis, or that this dry habitat was not a preferred habitat for M. ravelobensis due to other reasons. Thus, it cannot be excluded that the feeding niche differentiation of the two species and the reduced dietary width of M. ravelobensis in the zone of sympatry is the result of two independent evolutionary pathways and adaptations to different historic environments (overview in Townsend et al. 2002). To summarize, past or ongoing

62 Chapter 5 General discussion interspecific competition may have had implications for the coexistence of M. murinus and M. ravelobensis by influencing the feeding niche differentiation in zones of coexistence. The relative low population densities of the species with the lower competitive potential, M. ravelobensis, in the preferred dry habitats of the competitively dominant M. murinus might be explained by higher energetic costs when ensuring access to preferred resources despite the presence of the competitor.

5.2.2 Implications for varying regional abundance & geographic range size The outcome of interspecific interactions between competing species may influence their spatial distribution in heterogeneous environments (Case et al. 2005; Magnusson et al 1979; Montgomery 2009; Rowley & Christian 1976). For instance, in the sympatric microtine rodents Microtus montanus and M. longicaudus, the comparatively stronger males of M. montanus got access to habitats preferred by both species (Randall, 1978). Competitive advantage in geographically restricted species should allow them to maintain their often specialized ecological niches in the presence of widely distributed generalists (Miller 1967, mammals: Glazier & Eckert 2002; Hallett 1982). In contrast, M. ravelobensis was shown to have a lower competitive potential than M. murinus. However, even though M. ravelobensis is geographically restricted, it is not as specialized as predicted from its small geographic range size, and thus might therefore not require a high competitive potential to gain access to food resources. The locally specialized ecological niche of M. murinus in northwest may instead have been secured by the high competitive potential in this species. A high competitive ability may furthermore have enabled the range expansion of this widely distributed species (Darwin 1859; Brown 1984; Hanski 1982; Holway 1999; Walck et al. 1999; Wilson & Keddy 1986). In M. murinus, an elevated competitive potential may have enabled this species to expand geographically despite the presence of other competing species (Schneider et al. 2010). To summarize this section, the interspecific difference in competitive potential may be one among other factors that can explain the varying abundance of the two partial mouse lemurs in northwestern Madagascar. The higher competitive potential in the locally rarer M. murinus may enable this species to ensure access to preferred resources in suitable habitats in the region of coexistence of the two mouse lemur species. This high competitive potential might furthermore have enabled M. murinus to reach and maintain its wider distribution in northwestern Madagascar.

63 Chapter 5 General discussion

5.3 Conclusions

In this doctoral thesis I used two mouse lemur species, M. murinus and M. ravelobensis, as primate models to investigate whether resource use and interspecific competition can explain the coexistence and the interspecific differences in geographic distribution of two sympatric congeneric species in Madagascar. Their coexistence appears to be facilitated by a combination of interspecific feeding niche differentiation and reduced competition over available food resources due to reduced energetic needs in M. murinus. The two species showed different competitive potentials, and it is possible that the observed feeding niche differences were the result of past or ongoing competition. M. murinus and M. ravelobensis are found in varying abundances in the region of coexistence in northwestern Madagascar. This region is characterized by three different types of habitats: dry, intermediate and humid habitats, and the two species show differences in how they are distributed in these types of habitats. Whereas M. ravelobensis is found in highest densities in the intermediate and humid habitats, M. murinus is found in highest densities in dry habitat and is often absent in humid habitats (Rakotondravony & Radespiel 2009). Thus, habitat heterogeneity plays a major role in density regulation of the two mouse lemur species in northwestern Madagascar. Previous studies suggested that the bias in habitat use can be attributed to interspecific differences in sleeping site ecology (Rendigs et al. 2003). The results from this doctoral thesis suggest that the difference in habitat preference can also be attributed to interspecific differences in feeding strategies. Dry-adapted resource use in M. murinus might explain its higher densities in the dry habitats in northwest. Despite the higher competitive ability of M. murinus, this species is found in low abundance or is often absent in the more humid habitats, which suggests that these habitats are not suitable for this species. Tree holes for sleeping sites have been suggested to be a limiting resource for female M. murinus (Lutermann 2010). The restricted availability of tree holes in more humid areas may explain why they are not suitable habitats for M. murinus. The low competitive potential and/or different feeding strategies may explain the relatively low densities of M. ravelobensis in the dry habitats compared to M. murinus. In addition, humid-adapted resources use in M. ravelobensis may explain its high densities in these types of habitats. Possibly, high fruit productivity in humid habitats might furthermore enable higher population densities of this species in these conditions. It is possible that the ability of M. murinus to survive in dry habitats combined with its high competitive ability, has allowed this species to expand spatially over a large geographic range,

64 Chapter 5 General discussion e.g. via the drier highland areas of Madagascar. In contrast, the requirement of more humid habitat types for M. ravelobensis may have restricted the distribution of this species to the more humid regions in northwestern Madagascar.

5.4 References

Abramsky Z, Rosenzweig ML, Subach A. 2001. "The cost of interspecific competition in two gerbil species." J Anim Ecol 70:561-567. Azevedo FCC, Lester V, Gorsuch W, Lariviere S, Wirsing AJ, Murray DL. 2006. Dietary breadth and overlap among five sympatric prairie carnivores. J Zool 269:127-135. Amarasekare P. 2003. Competitive coexistence in spatially structured environments: a synthesis. Ecol Lett 6:1109-1122. Behmer ST, Joern A. 2008. Coexisting generalist herbivores occupy unique nutritional feeding niches. Proc Nat Acad Sci 105:1977. Bernstein IS. 1981. Dominance: the baby and the bathwater. J Behav Brain Sci 4:419-457. Bock CE. 1984. Geographical correlates of abundance vs. rarity in some North American winter landbirds. The Auk 101:266-273. Brändle M, Prinzing A, Pfeifer R, Brandl R. 2002. Dietary niche breadth for Central European birds: correlations with species-specific traits. Evol Ecol Res 4:643-657. Brown Jr WL, Wilson EO. 1956. Character displacement. Syst Zool 5:49-64. Brown JH. 1984. On the relationship between abundance and distribution of species. Am Nat 124:255-279. Brown JH. 1995. Macroecology. Univ. Chicago Press, Chicago. 270 pp. Case TJ, Holt RD, McPeek MA, Keitt TH. 2005. The community context of species„ borders: ecological and evolutionary perspectives. OIKOS 108: 28-46 Chase JM, Leibold MA. 2003. Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago, 212 pp. Corbin GD, Schmid J. 1995. Insect Secretions Determine Habitat Use Patterns by a Female Lesser Mouse Lemur (Microcebus murinus). Am J Primatol 37:317-324.

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Dammhahn M & Kappeler PM. 2008a. Small-scale coexistence of two mouse lemur species (Microcebus berthae and M, murinus) within a homogeneous competitive environment. Oecologia 157:473-483. Dammhahn M., Kappeler PM. 2008b. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29:1567-1589. Dammhahn M, Kappeler PM. 2010. Scramble or contest competition over food in solitarily foraging mouse lemurs (Microcebus spp.): New insights from stable isotopes. Am J Phys Anthropol 141:181-189. Dausmann KH, Glos J, Ganzhorn JU, & Heldmaier, G. 2005. Hibernation in the tropics: lessons from a primate. J Comp Physiol B 175: 147-155. Darwin C. 1859. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. 1st edn. John Murray, London. Eeley HAC, Foley RA. 1999. Species richness, species range size and ecological specialisation among African primates: geographical patterns and conservation implications. Biodiversity and Conservation 8:1033-1056. Garcia JT, Arroyo BE. 2005. Food-niche differentiation in sympatric Hen Circus cyaneus and Montagu's Harriers Circus pygargus. Ibis 147:144-154. Gause GF. 1934. The struggle for existence. Williams & Wilkins, Baltimore, MD, 460 pp. Génin F. 2004. Female dominance in competition for gum trees in the grey mouse lemur. Revue d‟Ecologie (la Terre et la Vie) 58: 397–410. Glazier DS. 1980. Ecological shifts and the evolution of geographically restricted species of North American Peromyscus (mice). J Biogeogr 7:63-83. Glazier DS, Eckert SE. 2002. Competitive ability, body size and geographical range size in small mammals. J Biogeogr 29:81-92 Hallett JG. 1982. Habitat selection and the community matrix of a desert small-mammal fauna. Ecol 63:1400-1410. Hanski I. 1982. Dynamics of regional distribution: the core and satellite species hypothesis. OIKOS 38:210-221. Harcourt AH, Coppeto SA, Parks SA. 2002. Rarity, specialization and extinction in primates. J Biogeogr 29:445-456. Harcourt AH, Coppeto SA, Parks SA. 2005. The distribution–abundance (density) relationship: its form and causes in a tropical mammal order, Primates. J Biogeogr 32:565-579.

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Hardin G. 1960. The competitive exclusion principle. Science 131:1292-1297. Harvey PH, Pagel MD. 1991. The comparative method in evolutionary biology: Oxford university press Oxford, 239 pp. Heino J. 2005. Positive relationship between regional distribution and local abundance in stream insects: a consequence of niche breadth or niche position? Ecography 28:345-354. Hladik CM, Charles-Dominique P, Petter JJ. 1980. Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar In: P Charles-Dominique, HM Cooper, A Hladik, CM. Hladik, E Pages, GF Pariente, A Petter-Rousseaux, A Schilling, JJ Petter, editors. Nocturnal Malagasy primates: ecology, physiology and behaviour. New York: Academic Press, p. 41-73. Holway DA. 1999. Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecol 80:238-251. Houle A, Vickery WL, Chapman CA. 2006. Testing mechanisms of coexistence among two species of frugivorous primates. J Anim Ecol 75:1034-1044. Hutchinson GE. 1957. Concluding remarks. Cold Springs Harbor Symp. Quant. Biol 22:415-427. Kaufmann JH. 1983. On the definitions and functions of dominance and territoriality. Biol Rev 58:1-20. Kobbe S, Dausmann KH. 2009. Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge. Naturwissenschaften 96:1221-1227. Komonen A, Grapputo A, Kaitala V, Kotiaho JS, Päivinen J. 2004. The role of niche breadth, resource availability and range position on the life history of butterflies. Oikos 105:41-54. Kotler BP, Brown JS, Subach A. 1993. Mechanisms of species coexistence of optimal foragers: temporal partitioning by two species of sand dune gerbils. Oikos 67: 548-556. Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS. 2005. Host specificity and geographic range in haematophagous ectoparasites. Oikos 108:449-456. 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. J of Zool 271:88-98. Lutermann H, Verburgt L, Rendigs A. 2010. Resting and nesting in a small mammal: sleeping sites as a limiting resource for female grey mouse lemurs. Anim Behav 79:1211-1219. Magnuson JJ, Crowder LB, Medvick PA. 1979. Temperature as an ecological resource. Integr Comp Biol 19:331.

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Marshall AJ, Wrangham RW. 2007. Evolutionary Consequences of Fallback Foods. Int J Primatol 28:1219-1235. Miller RS. 1967. Pattern and processes in competition. Advances in Ecological Research, 4:1–74. Montgomery WI. 2009. Population structure and dynamics of sympatric Apodemus species (Rodentia muridae). J Zool 192:351-377. Morin X, Chuine I. 2006. Niche breadth, competitive strength and range size of tree species: a trade off based framework to understand species distribution. Ecol Lett 9:185-195. Pagel MD, May RM, Collie AR. 1991. Ecological aspects of the geographical distribution and diversity of mammalian species. Am Nat 137:791-815. Pianka ER. 1973. The Structure of Lizard Communities. Annu Rev Ecol Syst 4:53-74. Porter LM. 2001. Dietary differences among sympatric Callitrichinae in northern Bolivia: Callimico goeldii, Saguinus fuscicollis and S. labiatus. Int J Primatol 22:961-992. Pyron M. 1999. Relationships between geographical range size, body size, local abundance, and habitat breadth in North American suckers and sunfishes. J Biogeogr 26:549-558. Radespiel U. 2006. Ecological diversity and seasonal adaptations of mouse lemurs (Microcebus spp.). In L Gould, ML Sauther, editors. Lemur ecology and adaptation. New York: Springer, p. 211-233. Rakotondravony R, Radespiel U. 2009. Varying patterns of coexistence of two mouse lemur species (Microcebus ravelobensis and M. murinus) in a heterogeneous landscape. Am J Primatol 71:928-938. Randall JA. 1978. Behavioral mechanisms of habitat segregation between sympatric species of Microtus: habitat preference and interspecific dominance. Behav Ecol Sociobiol 3:187- 202. Rendigs A, Radespiel U, Wrogemann D, Zimmermann E. 2003. Relationship between microhabitat structure and distribution of mouse lemurs (Microcebus spp.) in Northwestern Madagascar. Int J Primatol 24:47-64. Rowley MH, Christian JJ. 1976. Interspecific aggression between Peromyscus and Microtus females: a possible factor in competitive exclusion1. Behav Biol 16:521-525. Sandlin EA. 2000. Cue use affects resource subdivision among three coexisting hummingbird species. Behav Ecol 11:550-559. Schneider N, Chikhi L, Currat M, Radespiel U. 2010. Signals of recent spatial expansions in the grey mouse lemur (Microcebus murinus). BMC Evol Biol 10:105.

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Schmid J. 1999. Sex-specific differences in activity patterns and fattening in the gray mouse lemur (Microcebus murinus) in Madagascar. J Mammal:749-757. Schmid J. 2000. Daily torpor in the grey mouse lemur (Microcebus murinus) in Madagascar: Energetical consequences and biological significance. Oecologia 123:175–183. Schmid J, Kappeler PM. 2005. Physiologieal adaptations to seasonality. In: DK Brockman, CP van Schaik, editors. Primate Seasonality: Implications for Human Evolution. Cambridge: Cambridge University Press, p. 129-155. Schmid J, Ganzhorn JU. 2009. Optional strategies for reduced metabolism in gray mouse lemurs. Naturwissenschaften 96:737-741. Schoener TW. 1983. Field experiments on interspecific competition. Am Nat 122:240-285. Schülke O, Ostner J. 2007. Physiological ecology of cheirogaleid primates: variation in hibernation and torpor. Acta Ethologica 10:13-21. Shelley EL, Tanaka MYU, Ratnathicam AR, Blumstein DT. 2004. Can Lanchester's laws help explain interspecific dominance in birds? Condor 106:395-400. Sushma HS, Singh M. 2006. Resource partitioning and interspecific interactions among sympatric rain forest arboreal mammals of the Western Ghats, India. Behav Ecol 17:479. Townsend C, Harper J, Begon M. 2002. Ökologie. Berlin, Springer, 647 pp. Travaini A, Donázar JA, Rodríguez A, Ceballos O, Funes M, Delibes M, Hiraldo F. 1998. Use of European hare (Lepus europaeus) carcasses by an avian scavenging assemblage in Patagonia. J Zool 246:175-181. Walck JL, Baskin JM, Baskin CC. 1999. Relative competitive abilities and growth characteristics of a narrowly endemic and a geographically widespread Solidago species (Asteraceae). Am J Bot 86:820-828. Wilson SD, Keddy PA. 1986. Species competitive ability and position along a natural stress/disturbance gradient. Ecol 67:1236-1242. Ziv Y, Abramsky Z, Kotler BP, Subach P. 1993. Interference competition and temporal and habitat partitioning in two gerbil species. Oikos 66: 237-246.

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6

Summary

71 Chapter 6 Summary

Thorén, Sandra. Comparative feeding ecology of two sympatric mouse lemurs (Microcebus spp.) in northwestern Madagascar

In this doctoral thesis the golden-brown mouse lemur (Microcebus ravelobensis) and the gray mouse lemur (Microcebus murinus) were used as models to investigate whether interspecific differences in resource use and differences in competitive potential can explain coexistence and pronounced differences in geographic range size of sympatric congeneric primates in Madagascar. Since food is thought to be the most limiting resource of reproductive success in females, but not of males (Trivers 1972), this study focused on females. Because closely related species are likely to be ecologically similar due to common ancestry, they should show some degree of niche differentiation in order to coexist. Chapter 2 investigates whether temporal food partitioning and variable activity pattern can explain the coexistence of M. murinus and M. ravelobensis in northwestern Madagascar. Feeding and activity data were obtained by focal observations of 11 M. murinus and nine M. ravelobensis individuals during 11 months from 2007 to 2008, and by fecal sampling during six of these months. Food availability was determined by monitoring phenology of 272 plant specimens and trapping of arthropods. The results revealed that jointly used food resources were used to a different extent over the seasons by the congeneric species, resulting only in a partial dietary overlap. In addition, M. murinus showed a reduction in locomotor activity during the early dry season, which might reflect reduced energetic costs and thus lowered competition with M. ravelobensis over limited food resources. To conclude, a combination of interspecific feeding niche differentiation and reduced energetic requirements of M. murinus during the early dry season may facilitate the coexistence of M. murinus and M. ravelobensis even at times of limited resource abundance. A high competitive potential may entail advantages during resource acquisition. Thus, the outcome of interspecific competition may have implications for the reproductive success and thus potentially for the geographic distribution in species (Brown, 1984; Hanski, 1982). Chapter 3 therefore investigates the relative competitive potential of M. murinus and M. ravelobensis by testing 14 interspecific pairs in a two-cage experimental setup. Following two days of habituation, one 1-hour long encounter experiments were conducted daily for four days in a row. In general, the M. murinus individuals won significantly more conflicts than their cage partners. In eight of the 14 tested pairs, one individual won significantly more conflicts than the other, and in 87.5% of these dyads, M. murinus was the “dyad winner”. “Dyad winners” spent more time

72 Chapter 6 Summary feeding (p<0.05) and were less spatially restricted than “dyad losers” (p<0.05). To conclude, the high competitive potential in M. murinus might have enabled this species to expand geographically, despite the presence of other competing congeners. Interspecific differences in resource use might contribute to the understanding of how different species may coexist locally, but might also explain large-scale differences in geographic distribution patterns of species (Brown 1984). Chapter 4 investigates whether interspecific differences in the use of key food plant species and their varying distribution can explain the varying abundance of M. murinus and M. ravelobensis in northwestern Madagascar. To identify potential key plant species, feeding data from 17 female M. murinus and 18 female M. ravelobensis, and botanical data from 9 plots and 36 transects were obtained from three study sites. To test whether the varying abundance of the two congeners were influenced by the varying abundance of potential key plant species, trapping data of mouse lemurs and botanical data from the years 2003 to 2004 were analyzed from 18 study sites. Eight potential key food plant species of M. murinus and five of M. ravelobensis were identified. The varying abundance of three potential key plant species of M. murinus, but none of the potential key plant species of M. ravelobensis, was linked to the varying abundance of these mouse lemur species. Whenever any of these three potential key plant species of M. murinus were present, the probability to find M. murinus was 75-100%. The two congeners utilized different items of their potential key plant species. Whereas M. ravelobensis only consumed fruits, M. murinus showed a wider use of these plant species. M. murinus consumed fruits and buds as well as gum, which is a food resource thought to be especially important in environments where fruiting is irregular (Génin 2004). To conclude, M. murinus might have a feeding strategy adapted to dry habitats, whereas M. ravelobensis might rely more on humid habitats, which may explain the varying regional abundance of the sympatric species, and their pronounced differences in geographic range size throughout Madagascar. This doctoral thesis shows that an interspecific bias in competitive potential and interspecific differences in feeding strategies (feeding niches, activity pattern, seasonal changes in resource use) of M. murinus and M. ravelobensis, two sympatric congeners, may explain (a) their varying abundance in the heterogeneous landscapes in northwestern Madagascar, and (b) their pronounced differences in spatial distribution throughout Madagascar.

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Zusammenfassung

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Thorén, Sandra. Vergleichende Nahrungsökologie zweier sympatrischer Mausmakis (Microcebus spp.) im Nordwesten Madagaskars

In dieser Doktorarbeit wurden zwei Mausmakis (der Goldbraune Mausmaki, Microcebus ravelobensis und der Graue Mausmaki, Microcebus murinus) als Modell verwendet, um festzustellen, ob die Koexistenz und die ungleiche geografische Verteilung von sympatrischen artverwandten Primaten in Madagaskar von interspezifischen Unterschieden in der Ressourcennutzung sowie der Wettbewerbsfähigkeit beeinflusst werden. Da Nahrung der limitierende Faktor bei Fortpflanzungserfolgen weiblicher Tiere sein soll - aber nicht bei Männchen (Trivers 1972) - wurden in dieser Studie ausschließlich weibliche Tiere untersucht. Eng verwandte Arten können aufgrund ihrer gemeinsamen Abstammung ökologische Ähnlichkeiten entwickeln und sollten eine gewisse Nischendifferenzierung aufweisen, um koexistieren zu können. In Kapitel 2 werden die zeitliche Nahrungsaufteilung sowie die unterschiedlichen Aktivitätsmuster untersucht, um festzustellen, ob diese Verhaltensweisen eine Erklärung für die Koexistenz von M. murinus und M. ravelobensis im Nordwesten Madagaskars darstellen. Von 2007 bis 2008 innerhalb von 11 Monaten wurden Daten zur Nahrungsaufnahme und Aktivität durch fokale Beobachtungen von 11 M. murinus- und neun M. ravelobensis- Individuen und innerhalb von sechs Monaten im gleichen Zeitraum Fäkalproben gesammelt. Durch die Identifikation der Phänologie von 272 Pflanzenproben und Arthropodenfang wurde das Nahrungsangebot ermittelt. Die Ergebnisse zeigen, dass gemeinsam verwendete Nahrungsquellen über die Jahreszeiten unterschiedlich genutzt wurden, wobei geringe partielle Üeberschneidungen stattfinden. Des Weiteren zeigte M. murinus eine Reduzierung der lokomotorischen Aktivität während der frühen Trockenzeit, was zu einer Reduzierung der energetischen Kosten und daher auch des Wettbewerbs mit M. ravelobensis um begrenzte Nahrungsressourcen führen könnte. Eine Kombination aus interspezifischen Nahrungsnischen und des reduzierten Stoffwechsels von M. murinus während der Trockenzeit könnte die Koexistenz von M. murinus und M. ravelobensis auch während Perioden begrenzter Nahrungsressourcen erleichtern. Ein hohes Potential an Wettbewerbsfähigkeit kann ein Vorteil für die Ressourcenbeschaffung darstellen. Daher kann der interspezifische Wettbewerb den Reproduktionserfolg und folglich auch die geografische Verteilung von Spezies beeinflussen (Brown, 1984; Hanski, 1982). In Kapitel 3 wird das relative Potential der Wettbewerbsfähigkeit von M. murinus und M. ravelobensis untersucht, indem 14 interspezifische Paare in einem

76 Chapter 7 Zusammenfassung

Zweikäfig-Versuch getestet werden. Nach einer zweitägigen Eingewöhnungszeit wurden einmal täglich für vier folgende Tage einstündige Konfliktversuche durchgeführt. M. murinus-Individuen haben signifikant mehr Konflikte als ihr Kontrahent gewonnen. In acht der 14 untersuchten Paare hat ein Individuum signifikant mehr Konflikte gewonnen; in 87.5% dieser Dyaden war M. murinus der “Dyaden-Sieger”. “Dyaden-Sieger” verbrachten mehr Zeit bei der Nahrungsaufnahme (p<0.05) und waren räumlich weniger begrenzt als „Dyaden-Verlierer“ (p<0.05). Es ist möglich, dass das hohe Potential der Wettbewerbsfähigkeit von M. murinus für ihre relativ weite geografische Verbreitung trotz der Anwesenheit konkurrierender artverwandter Spezies verantwortlich ist. Interspezifische Unterschiede der Ressourcennutzung kann zum Verständnis, wie die lokale Koexistenz verschiedener Spezies funktioniert, aber auch zum Verständnis der weiträumigen Unterschiede geografischer Verteilungsmuster von Spezies, beitragen (Brown 1984). In Kapitel 4 werden interspezifische Unterschiede in der Verwendung von Schlüssel- Pflanzenarten und deren Verbreitung dahingehend untersucht, ob diese einen Einfluss auf die unterschiedlichen Abundanzen von M. murinus und M. ravelobensis im Nordwesten Madagaskars haben könnten. Für die Bestimmung potentieller Schlüsselpflanzenarten wurden Nahrungsdaten von 17 weiblichen M. murinus- und 18 weiblichen M. ravelobensis-Tieren untersucht sowie botanische Daten von 9 Parzellen und 36 Transekten von Untersuchungsgebieten gesammelt. Des Weiteren wurden die Fangdaten beider Mausmakis sowie die botanischen Daten aus den Jahren 2003 bis 2004 von 18 Untersuchungsgebieten analysiert, um zu prüfen, ob die unterschiedlichen Abundanzen potentieller Schlüsselpflanzenarten einen Einfluss auf die unterschiedlichen Abundanzen beider Schwesterarten haben. Acht potentielle Schlüsselpflanzenarten von M. murinus und fünf von M. ravelobensis wurden identifiziert. Für M. ravelobensis konnten keine Verbindungen zwischen Schlüsselpflanzenabundanz und Speziesabundanz gefunden werden, aber für M. murinus dagegen konnten bei drei Schlüsselpflanzenarten eine Relation der Abundanzen nachgewiesen werden. Wann immer einer dieser Schlüsselpflanzenarten von M. murinus vorhanden war, war die Wahrscheinlichkeit, M. murinus zu finden 75-100%. Die beiden Schwesterspezies verwendeten unterschiedliche Teile ihrer potentiellen Schlüsselpflanzen. Im Gegensatz zu M. ravelobensis, die nur Früchte konsumierten, verspeisten M. murinus mehr Pflanzenanteile, wie Früchte, Knospen und Baumharz. Letzteres ist durchaus relevant in einer Umwelt mit unregelmäßiger Fruchtbildung (Génin 2004). M. murinus könnte eine an eine trockene Umwelt adaptierte

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Nahrungsstrategie besitzen, wobei M. ravelobensis mehr an feuchtere Habitate angepasst sein könnte. Darauf könnten die unterschiedlichen Abundanzen beider sympatrischen Spezies und die sehr unterschiedlichen geografischen Verteilungen beruhen. Diese Doktorarbeit zeigt, dass das interspezifische Ungleichgewicht des kompetitiven Potentials sowie die interspezifische Unterschiede der Nahrungsstrategien (Nahrungsnischen, Aktivitätsmuster, jahreszeitliche Änderungen der Ressourcennutzung) von M. murinus und M. ravelobensis, zwei sympatrische artverwandte Spezies, folgende Phänomene aufklären kann: (a) die unterschiedlichen Abundanzen in einer heterogenen Landschaft des Nordwestens von Madagaskar, und (b) die sehr unterschiedliche geografische Verteilung auf Madagaskar.

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Declaration

I herewith declare that I autonomously carried out the PhD-thesis entitled “Comparative feeding ecology of two sympatric mouse lemurs (Microcebus spp.) in northwestern Madagascar”.

I did not receive any assistance in return for payment by consulting agencies or any other person. No one received any kind of payment for direct or indirect assistance in correlation to the content of the submitted thesis.

I conducted the project at the Institute of Zoology at the University of Veterinary Medicine Hannover.

The thesis has not been submitted elsewhere for an exam, as thesis or for evaluation in a similar context.

I hereby affirm the above statements to be complete and true to the best of my knowledge.

Sandra Thorén

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Acknowledgements

81 Chapter 8 Acknowledgements

I would like to thank:

My supervisor Prof. Ute Radespiel, who despite my poor French and after a single phone interview, was brave enough to accept me as her PhD student. She provided me with excellent scientific support during my PhD study, encouraged me to believe in myself, to take responsibility and work independently.

Prof. Elke Zimmermann, the head of our department, for financial support during my last months of work, for her encouragement during these years, and for providing a pleasant and supportive work environment.

My two external supervisors, PD Dr. Björn Siemers and Prof. Hansjoachim Hackbarth, for helpful feedback on my PhD work. My external examinator Prof. Jörg Ganzhorn for attending my defense.

The Deutsche Forschungsgemeinschaft (DFG RA 502/9-1) for financial support.

Dr. Blanchard Randrianambinina, Dr. Solofo Rasoloharijaona and Romule Rakotondravony for their enormous help during my field work in Madagascar; not only for helping me to set up the field work, arranging research permits, working visas, but for their help with all kinds of unpredictable things that constantly happen in the field.

Lalandy Sehen, who spent a year in the field with me in Madagascar, for being such a nice, helpful and encouraging person, for sharing her botanical data with me, and also for patiently teaching me Malagasy and helping me in all possible way during my study.

Miriam Linnenbrink, who conducted her master thesis in field in Madagascar, for providing valuable data on interspecific competition, and for sharing a great time in field with me. Christopher Meusel, who conducted his master thesis at the Institute of Zoology, for analyzing fecal samples that had been collected during my time in field in Madagascar. Dr. Albert Melber for valuable help identifying arthropod taxa.

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Dr. Franziska Quietzsch who conducted her doctoral thesis in Madagascar, and her field assistant Sonja Kunath, for providing me with feeding data of M. ravelobensis, and for making life in the field and especially capturing of the mouse lemurs so enjoyable.

Doreen Schwochow, my field assistant, for providing excellent help during my first tough months in the field, for many good discussions and laughs, and for always doing her very best.

Kate Meares, my field assistant, for excellent help during my field work, for hours of discussions about anything and nothing, for proof reading and English corrections and for encouraging me to do whatever blows my hair back .

My other field assistants: Pièrre Razafindraibe, Fanomezantsoa Rakotonirina, Roger Randrimparany, Mananjara and Tosy for great help and expertise during data collection.

Other persons conducting field work at the field station, especially Pia Eichmüller for good friendship, Keriann McGoogan for support and for being such a great running and yoga partner, Travis Steffens for his enthusiam about everything, Rindrahatsarana Ramanankirahina and Sato Hiroshima for sharing great times.

The Department des Eaux et Forêts (DEF), the members of CAFF/CORE, the University of Antananarivo (D. Rakotondravony, O. Ramilijaona), and the Association pour la Gestion des Aires Protégées (ANGAP) for the permission to work in the Ankarafantsika National Park. The local staff in the National Park for their continuous support, and particulary to the people at ANGAP: René Razafindrajery, Rakotoarimanana Justin, Edouard Randriamanantsoa, Vanona Rafam'andrianjafy, Jacqueline Razaiarimanana. Special thanks go to Eric la Croix, for being so generous and helpful, the Durrell Wildlife Preservation Trust for providing the climatic data of Ampijoroa.

All my colleagues at the Institute of Zoology. A special thanks to Rüdiger Bruning for his excellent technical support and for helping make posters, Sönke von den Berg for being very helpful for providing me with figures and technical support, Brigitte Lohmeier for help transcribing data, Karsten Instenberg for help with computer and internet problems, Sandra

83 Chapter 8 Acknowledgements

Hamacher and Heike Held for help with all the administrational work, Hella Breitrück and Sabine Sippel for their kindness and great support.

Also, my colleagues Marina Scheumann, Lisette Leliveld and Christina Schopf for the nice time spent together during my PhD study, Sharon Kessler for proof reading parts of my thesis, and Mathias Craul for valuable help and for being such a great friend.

Marine Joly and Angie Faust, my stand-in family in Hanover, for great support and appreciated friendship. A special thanks to Marine for helping with all kind of administrative things when I was in Madagascar and to Angie for proof reading, English corrections and German translations.

My mentor, Prof. Kerstin Olsson, for her inspiring optimism and encouragement during all these years.

My beloved family: my sister, my parents and Egon for always supporting and encouraging me in every way and for telling me that life is full of possibilities.

The mouse lemurs in the field .

.

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Curriculum Vitae

85 Chapter 9 Curriculum vitae

CURRICULUM VITAE

SANDRA THORÉN

March 2011

Birth date: 24th of November 1976 Nationality: Swedish Email: [email protected] [email protected]

EDUCATION

Since Jan PhD study, Institute of Zoology, University of Veterinary Medicine Hanover, Germany. 2007 PhD topic: “Comparative feeding ecology of sympatric mouse lemurs in Ankarfantsika National Park, Madagascar”. Supervision: Prof. Ute Radespiel.

1999-2005 Master of Science in Biology, Swedish University of Agricultural Sciences, Uppsala, Sweden.

1999-2004 Master of Science in Agricultural Science (Animal), Swedish University of Agricultural Sciences, Uppsala, Sweden.

RESEARCH EXPERIENCE AND FIELDWORK

Since Jan Principal investigator. Comparative feeding ecology study of the gray mouse lemur 2007 Microcebus murinus) and the golden-brown mouse lemur (Microcebus ravelobensis), Ankarfantsika National Park, Madagascar. PhD research included 16 months field work, Institute of Zoology, University of Veterinary Medicine Hanover, Germany. Supervision: Ute Radespiel.

Jan-Feb Field assistant. Ecological study of Forest-falcons (Micrastur), Los Amigos Research 2006 Station and Conservation Area, Peru. PhD study of Ursula Valdez, University of Washington, USA.

Sept-Nov Field assistant. Behavioral study of the Monk saki monkeys (Pithecia monachus), 2005 Los Amigos Research Station and Conservation Area, Peru. Susan Palminteri, WWF, USA.

Oct-Nov Field assistant. Behavioral study of Brown titi monkeys (Callicebus brunneus), Los 2004 Amigos Research Station and Conservation Area, Peru. PhD study of Jenna Lawrence, Columbia University, USA.

86 Chapter 9 Curriculum vitae

April–Oct Principal investigator. Comparative feeding ecology study of the bonobo (Pan 2004 paniscus), the red colobus (Piliocolobus thalloni), the black mangabey (Lophocebus atterimus), the wolf’s monkey (Cercopithecus wolfi) and the red-tailed monkey (Cercopithecus ascanius), Salonga National park, DR Congo. MSc research included 3 months field work, Department of Zoology, Stockholm University, Sweden. Supervision: Assoc. Prof. Patrik Lindenfors. In collaboration with Dr. Gottfried Hohmann, Max Planck Institute, Leipzig, Germany.

June–Dec Principal investigator, Phylogenetic study of canine size and canine sexual size 2003 dimorphism in primates. MSc research, Department of Zoology, Stockholm University, Sweden. Supervision: Assoc. Prof. Patrik Lindenfors.

May-Sept Co-principal investigator, Physiological study investigating the correlation between 2003 behavior and hormone concentrations in blood plasma (oxytocin, vasopressin and cortisol) and estimated pain in kidding goats. Msc research, Department of Animal Physiology, Swedish University of Agricultural Sciences, Sweden. Supervision: Professor em. Kerstin Olsson.

April-June Principal investigator: Behavioral study of mice: evaluating recording techniques 2001 for activity measurements of mice in their home cages. Independent project, Department of Animal Physiology, Swedish University of Agricultural Sciences, Sweden. Supervision: Hanna Augustsson & Kristina Dahlborn.

PUBLICATIONS

2011 Thorén S, Miriam L & Radespiel U. Different competitive potential in two coexisting mouse lemur species in northwestern Madagascar. American Journal of Physical Anthropology 145: 156-162.

2011 Thorén S, Quietzsch F, Schwochow D, Sehen L, Meusel C, Meares K & Radespiel U. 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. International Journal of Primatology 32: 566-586.

2010 Sehen L, Goetze D, Rajeriarison C, Roger E, Thorén S & Radespiel U. Structural and floristic traits of habitats with differing relative abundance of the lemurs Microcebus murinus and M. ravelobensis in northwestern Madagascar. Ecotropica 16: 15-30.

2009 Thorén S, Quietzsch F & Radespiel U. Leaf nest use and construction in the golden- brown mouse lemur (Microcebus ravelobensis) in the Ankarafantsika National Park. American Journal of Primatology 71: 1-8.

2006 Thorén S, Lindenfors P & Kappeler PM. Phylogenetic analyses of dimorphism in primates - evidence for stronger selection on canine than on body size. American Journal of Physical Anthropology 130: 50-59.

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2004 Olsson K, Stein J & Thorén S. Correlation between behaviour during labour and blood plasma concentrations of vasopressin in goats. Journal of Animal and Feed Sciences 13: 543-546.

PUBLICATIONS SUBMITTED AND IN PREPARATION

Submit. Thorén S, Sehen L, Rakotondravony R, Quietzsch F, Radespiel U. Can the distribution of key food plants explain the varying abundance of two mouse lemur species (Microcebus spp.) in northwestern Madagascar? American Journal of Primatology.

Submit. Crowley BE, Thorén S, Rasoazanabary E, Barrett MA, Zohdy S, Blanco MB, McGoogan KC, Arrigo-Nelson SJ, Irwin MT, Vogel ER, Wright PC, Radespiel U, Godfrey LR, Koch PL, Dominy NJ. Geographic isotopic variation among mouse lemur (Microcebus) populations

CONFERENCE CONTRIBUTIONS

2011 Thorén S, Sehen L, Rakotondravony R & Radespiel U. Can key food resources explain the presence and absence of two mouse lemurs (Microcebus spp.) in northwestern Madagascar? Annual Conference of the Society for Tropical Ecology, Frankfurt, Germany.

2010 Thorén S, Sehen L, Rakotondravony R & Radespiel U. Comparative feeding ecology of two sympatric mouse lemurs (Microcebus spp.) in northwestern Madagascar. 23rd Congress of International Primatological Society, Kyoto, Japan.

2009 Thorén S, Linnenbrink M & Radespiel U. Investigation of inter-specific dominance pattern between two sympatric mouse lemurs in north-western Madagascar. 31st International Ethological Conference, Rennes, France.

2009 Thorén S, Linnenbrink M & Radespiel U. Experiments on interspecific food competition in two coexisting mouse lemur species in north-western Madagascar. 3rd Congress of the European federation for primatology, Zurich, Switzerland.

2009 Thorén S & Radespiel U. The influence of seasonality on activity, feeding ecology and feeding niche differentiation in two sympatric mouse lemurs in the Ankarafantsika National Park, northwestern Madagascar. 11th Meeting of the Gesellschaft für Primatologie, Hanover, Germany.

2008 Thorén S, Schowochow D, Quietzsch F, Kunath S & Radespiel U. Leaf nest usage in the golden-brown mouse lemur (Microcebus ravelobensis) in Ankarafantiska National Park. 22nd Congress of the International Primatological Society, Edinburgh, Scotland.

2008 Linnenbrink M, Thorén S & Radespiel U. Inter-specific dominance between two sympatric mouse lemurs (Microcebus murinus and M. ravelobensis) in northwestern Madagascar. Jahrestagung der Ethologischen Gesellschaft, Regensburg, Germany.

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