University of Veterinary Medicine Hannover Institute of Zoology

The evolution of social dominance in mouse lemurs (Microcebus spp.): the effect of sex and species on social interaction

THESIS

Submitted in partial fulfilment of the requirements for the degree

DOCTOR OF PHILOSOPHY (PhD)

awarded by the University of Veterinary Medicine Hannover by Rina Evasoa Mamy Antananarivo, Madagascar

Hannover, Germany 2018

Supervisor: Prof. Dr. Elke Zimmerman Prof. Dr. Ute Radespiel

Supervision Group: Prof. Dr. Elke Zimmerman Prof. Dr. Ute Radespiel PD. Dr. Heike Hadrys Prof. Dr. Julia Ostner

1st evaluation: Prof. Dr. Elke Zimmerman University of Veterinary Medicine Hannover, Institute of Zoology

Prof. Dr. Ute Radespiel University of Veterinary Medicine Hannover Institute of Zoology

PD. Dr. Heike Hadrys University of Veterinary Medicine Hannover Institute for Animal Ecology and Cell Biology

Prof. Dr. Julia Ostner Department of Behavioral Ecology Georg-August-University Göttingen

2nd evaluation: Prof. Dr. Cristina Giacoma University of Torino. Dept. of Life Sciences and System Biology, V. Accademia Albertina, 13. 10123 Torino, Italy Date of final exam: 29.10.2018 Part of the thesis has been published previously in: American Journal of Primatology Sponsorship: DAAD

Great is our Lord, and of great power: his understanding is infinite.

Psalms 147:5

To

my parents

my husband

my sister

my brother

my nephew

Table of contents

Table of contents …………………………………………………………………………….. i List of figures………………………………………………………………………………… iii List of tables………………………………………………………………………………….. iv Previously published excerpts of this thesis…………………………………………………. v Summary……………………………………………………………………………………... vii Zusammenfassung……………………………………………………………………………. ix

Chapter 1 – General introduction 1 1.1 Background……………………………………………………………………………. 1 1.2 Social tolerance and social relationship in primates…………………………………... 2 1.2.1 Affiliation …………………………………………………………………………...... 2 1.2.2 Agonistic behavior …………………………………………………………………...... 3 1.3 The evolution of social dominance…………………………………………………….. 3 1.4 The evolution of social tolerance and female dominance……………………………… 4 1.5 Mouse lemurs (Microcebus spp.)……………………………………………………..... 6 1.6 Anthropogenic pressures and threats acting on mouse lemur populations and species... 11 1.7 Aims and hypotheses………………………………………………………………….. 12

Chapter 2 - Variation in reproduction of the smallest‐bodied primate radiation, the mouse lemurs (Microcebus spp.): A synopsis 14

Chapter 3 – Determinants of interspecific variation in social tolerance in mouse lemurs (Microcebus spp.) 15 3.1 Introduction…………………………………………………………………………... 16 3.2 Results ………………………………………………………………………………... 19 3.2.1 Variation of affiliation during the encounters among dyad types and species ………. 19 3.2.2 Variation in rates of agonism and number of conflicts among dyad types and species.. 23 3.2.3 Variation in social dominance among dyad types and species……………………….. 26 3.3 Discussion…………………………………………………………………………….. 28 3.3.1 Influence of phylogeny on social tolerance…………………………………………... 29 3.3.2 Influence of habitat type on social tolerance…………………………………………. 31 3.3.3 Influence of reproductive activity on social tolerance………………………………... 32 3.3.4 Interspecific variability in social tolerance and implications for social diversity mouse lemurs………………………………………………………………………….. 33 3.4 Conclusions…………………………………………………………………………… 36 3.5 Methods……………………………………………………………………………….. 36 3.5.1 Study sites and study species…………………………………………………………. 36 3.5.2 Capture and selection of study animals……………………………………………….. 37 3.5.3 Experimental set-up and data collection……………………………………………… 38 3.5.4 Behavioral observations………………………………………………………………. 38 3.5.5 Statistical modelling…………………………………………………………………... 40 3.6 Declarations…………………………………………………………………………… 41 3.6.1 Ethics approval………………………………………………………………………... 41 i

3.6.2 Consent for publication………………………………………………………………. 41 3.6.3 Availability of data and material……………………………………………………… 41 3.6.4 Competing interests…………………………………………………………………… 41 3.6.5 Funding………………………………………………………………………………... 41 3.6.6 Author’s contributions………………………………………………………………… 42 3.7 Acknowledgements…………………………………………………………………….. 42 3.8 References……………………………………………………………………………… 42 3.9 Additional files ………………………………………………………………………… 48

Chapter 4- General discussion 64 4.1 Reproductive plasticity in mouse lemurs……………………………………………… 65 4.2 Social plasticity in mouse lemurs…………………………………………………….. 67 4.3 Plasticity in female dominance among mouse lemurs ………………………………. 69 4.4 Implications for taxonomy……………………………………………………………. 72 4.5 Implications for conservation………………………………………………………… 72 4.6 Outlook………………………………………………………………………………… 72

Chapter 5 – References for introduction and discussion 73

Acknowledgments 84 AFFIDAVIT 88

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List of figures

Figure 1.1 Distribution map for Microcebus spp………………………………………… 8 Figure 1.2 Picture of six study species (Microcebus spp.)………………………………. 9 Figure 3.1 Species comparison of the joint use of sleeping box………………………… 20 Figure 3.2 Species comparison of joint space use per dyad type ………………………. 22 Figure 3.3 Species comparison of total body contact per dyad type ………………….. 23 Figure 3.4 Aggression rates in mf-dyads for each species and sex separately………… 24 Figure 3.5 Aggression rates in mm-dyads for each forest type…………………………. 25 Figure 3.6 Species comparison of the total number of conflicts per dyad type. ………. 26 Figure 3.7 Map with northern half of Madagascar showing study sites of six study species………………………………………………………………………… 37 Figure 3.8 Encounter cage with eight compartments (A-H) and four extra locations (Ro, T, S, FS)………………………………………………………. 38 Figure 4.1 Evolution of seasonality and aseasonality reproduction pattern in lemur species………………………………………………………………………… 67 Figure 4.2 Partial clade showing evolution of female dominance in lemurs…………….. 71

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List of tables

Table 1.1 Distribution of different types of female dominance among lemur……………… 5 Table 3.1 Number of won conflicts for males and females in male-female dyads and their statistical comparison …………………………………………………………..... 27 Table 3.2 Number of male-male-dyads with significant male-male dominance per species 27 Table 3.3 Summary of findings on parameters that explained variation in social tolerance and its outcome …………………………………………………………………. 30 Table 3.4 Descriptive data of study species ………………………………………………... 48 Table 3.5 Statistical model for staying together in the sleeping box………………………. 49 Table 3.6 Statistical models for joint space use……………………………………………. 50 Table 3.7 Statistical models for total body contact………………………………………… 53 Table 3.8 Statistical model for aggression rate……………………………………………... 55 Table 3.9 Statistical models for number of conflicts……………………………………….. 57 Table 3.10 Summary of decided conflicts…………………………………………………. 60

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Previously published excerpt of this thesis

Chapter 2 of this thesis was published in the scientific peer-reviewed journal American Journal of Primatology.

Publications:

Chapter 2 was published on 16th August 2018 in the journal “American journal of primatology” entitled “Variation in reproduction of the smallest‐bodied primate radiation, the mouse lemurs (Microcebus spp.): a synopsis.” by Mamy Rina Evasoa, Ute Radespiel, Alida Frankline Hasiniaina, Solofonirina Rasoloharijaona , Blanchard Randrianambinina , Romule Rakotondravony , Elke Zimmermann (Volume 80 issue 7; DOI: 10.1002/ajp.22874). It was first published online on 16th May 2018. The copyright is held by John Wiley and Sons.

The American journal of primatology is the original source of publication which can be accessed on https://onlinelibrary.wiley.com/doi/abs/10.1002/ajp.22874. The format of the chapter was adapted to the style of this thesis.

The conception and design of the study presented in chapter 2 were performed by MRE, EZ and UR. The data were collected by MRE and AFH. The interpretation of the data was done by MRE, EZ and UR. The article was drafted by MRE, EZ, and critically revised by all authors. All authors approved the publication of the final version.

Chapter 3 represents a manuscript, which is submitted to a scientific peer-reviewed journal of publication in BMC Ecology by Mamy Rina Evasoa, Elke Zimmermann, Alida Frankline Hasiniaina, Solofonirina Rasoloharijaona, Blanchard Randrianambinina, Romule Rakotondravony and Ute Radespiel.

The conception and design of the study presented in chapter 3 was performed by MRE, EZ and UR. EZ and UR conceived and designed the study. MRE and AFH collected the data. MRE and UR analyzed the data and drafted the manuscript. All authors participated in the interpretation of the data. All authors read and approved the final manuscript.

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Poster/ Presentations at scientific meetings:

Rina Evasoa M., Hasiniaina A. F., Rasoloharijaona S., Randrianambinina B., Radespiel U., & Zimmermann E. (2017). “Variation in Intra-and Intersexual relationships in closely related species of a nocturnal primate radiation”. (Microcebus spp.). 7th European Federation for Primatology (EFP) meeting. University of Strasbourg, France. August 21-25, 2017.

Rina Evasoa M., Hasiniaina A. F., Randrianambinina B., Rasoloharijaona S., Radespiel U., & Zimmermann E. (2017). “Reproductive variation in the large radiation of the smallest primates, mouse lemurs (Microcebus ssp.)”. Inaugural Madagascar Primatological Society Congress, Madagascar. December 13 – 16, 2017.

Rina Evasoa M., Zimmermann E., Hasiniaina A. F., Randrianambinina B., Rasoloharijaona S., &. Radespiel U. (2018). “Is there a relationship between aggression levels, reproductive seasonality and habitat in mouse lemurs (Microcebus ssp.)?” 27th International Primatological Society Congress, Nairobi, Kenya. August 19 – 25, 2018.

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Summary Rina Evasoa Mamy The evolution of social dominance in mouse lemurs (Microcebus spp.): the effect of sex and species on social interaction.

Reproduction is a fundamental trait in the life history of any species and contributes to species diversity and evolution. In mammals, social behavior plays an important role for reproduction and its coordination. In diurnal primates, with their complex societies, egalitarian to despotic social relationships are established and maintained via agonistic conflicts, allogrooming, coalitions, as well as by spatial affiliation. Thereby, social tolerance is a very important concept, strongly influencing the patterns of affiliation and aggression in group-living species. In contrast to our knowledge on the evolution of social relationships in group-living, diurnal primates, our knowledge on nocturnal species living in dispersed social systems is very limited.

The aim of this thesis is to fill this gap by investigating interspecific variation of reproductive schedules and social tolerance in 12 species of a closely related, highly speciose nocturnal lemur radiation the mouse lemur, which live in socially dispersed social systems. In a first study, I investigated differences in the reproductive schedule of these mouse lemur species and how they can be explained by phylogenetically and/or ecological factors. In a second study, I investigated how social tolerance is affected by phylogeny, ecology, and reproductive activity by exploring the variation in inter-sexual (male-female) and intra-sexual (male-male) interactions of six closely related species (Microcebus myoxinus, M. lehilahytsara, M. mamiratra, M. margotmarshae, M. ravelobensis, M. bongolavensis and M. danfossi), using a standardized social encounter paradigm.

For the first study, the variation in reproductive schedules was assessed in 12 species of the smallest-bodied primate radiation (Microcebus spp.) by compiling literature records on reproduction for four species, by analyzing long-term data from the working group Zimmermann/Radespiel for two species, and by assessing reproductive status for further six species in Madagascar. To assess the reproductive status, testes size was measured for males, vaginal cytology and teat status was documented for females. Based on existing literature, the study species were assigned to four phylogenetic clades, characterized by forest type (dry forest, humid forest) and with regard to environmental parameters such as day length fluctuations, temperature, and yearly rainfall. The results showed that the 12 species differed

vii in their reproductive schedule and that this variation could be best explained by an interplay between phylogenetic relatedness and forest type.

For the second study, I evaluated the interspecific variation in social tolerance in six mouse lemur species (Microcebus spp.) by assessing inter-individual patterns of affiliative and agonistic behavior as well as social dominance in experimentally formed social dyads with a standardized social encounter paradigm. The six different mouse lemur species belong to three different clades, inhabit two contrasting habitats (dry vs humid forest), and differed regarding their reproductive state. Six male-female pairs and six male-male pairs of each species were observed during the standardized social encounter experiments over three hours/a day at the beginning of the night for six days. The joint stay in sleeping box, the joint use of space, frequency of non-agonistic body contacts, aggression rates, and the number of intra-sexual and intersexual conflicts were quantified and analysed. The results showed different levels of social tolerance in the six mouse lemur species. This variation was significantly affected by habitat type and reproductive activity, but less influenced by phylogeny.

All in all, the two studies provided a new insight into the divergence in reproductive schedules, which supports the taxonomic distinctiveness of these mouse lemur species. Moreover, the regulation of social tolerance varied considerably across species. Although both reproductive schedule and social tolerance were affected by ecological factors, ecology was not a sufficient variable to explain interspecific variations. Instead, an interplay between ecology and phylogeny for reproductive schedule and an interplay between reproductive activity and ecology for social tolerance was important to explain the observed inter-specific variations in reproductive schedule and social tolerance. Thus, the findings suggest that current ecological hypotheses are insufficient to explain the complex relations between ecology, reproduction, and aggression in this primate radiation. Thus, further studies are needed on all lemur species in different reproductive states.

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Zusammenfassung

Rina Evasoa Mamy Die Evolution sozialer Dominanz in Mausmakis (Microcebus spp.): Die Auswirkung von Geschlecht und Arten auf die soziale Interaktion.

Die Reproduktion ist ein grundlegendes Merkmal der Life-history aller Arten, welches zur Artendiversität und Evolution beiträgt. Bei Säugetieren spielt das Sozialverhalten eine wichtige Rolle bei der Koordination der Reproduktion. Bei tagaktiven Primaten mit komplexen sozialen Systemen, basieren egalitäre und despotische soziale Beziehungen auf agonistischen Konflikten, gegenseitiger Fellpflege, Koalitionen und räumlicher Nähe. Dabei ist soziale Toleranz ein wichtiges Konzept, welches affiliative und agonistische Muster in gruppenlebenden Arten maßgeblich beeinflusst. Im Gegensatz zu unserem umfangreichen Wissen über die Evolution von Sozialbeziehungen bei tagaktiven Primaten, ist bislang wenig über nachtaktive Arten, die in verstreuten Sozialsystemen leben, bekannt.

Das Ziel dieser Arbeit ist es, diese Lücke zu füllen, indem die zwischenartliche Variation des zeitlichen Verlaufs der Reproduktion und die soziale Toleranz an 12 eng verwandten Arten untersucht wurden. Diese gehören einer artenreichen, nachtaktiven Lemurengruppe an und leben in verstreuten Sozialsystemen. In der ersten Studie habe ich untersucht, ob Unterschiede im jährlichen Verlauf der Reproduktion zwischen diesen Mausmakiarten auftreten und wie diese Variation durch phylogenetische und ökologische Faktoren erklärt werden können. In einer zweiten Studie habe ich untersucht, wie sich die soziale Toleranz zwischen sechs nah verwandten Mausmakiarten (Microcebus myoxinus, M. lehilahytsara, M. mamiratra, M. margotmarshae, M. ravelobensis, M. bongolavensis and M. danfossi) unterscheidet und wie diese Variation durch phylogenetische, ökologische und reproduktionsspezifischer Faktoren erklärt werden können. Hierzu habe ich intra- und intersexuelle Interaktionen unter Nutzung eines standardisierten sozialen Begegnungsexperimentes untersucht.

Für die erste Studie wurde die Variation im zeitlichen Ablauf der Reproduktion von 12 Mausmakiarten erfasst, indem für vier Arten Literatur herangezogen wurde, für zwei Arten Langzeitdaten der Arbeitsgruppe Zimmermann/Radespiel ausgewertet wurden und für sechs Arten neue Daten in Madagaskar erhoben wurden. Um den Reproduktionszustand zu erfassen, wurden bei den Männchen die Hoden vermessen während bei den Weibchen die Vaginalzytologie und der Zitzenstatus erfasst wurden. Basierend auf der Literatur wurden die untersuchten Arten vier phylogenetischen Clustern zugeordnet und durch ökologische

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Faktoren wie Waldhabitat, Tageslängenfluktuation, Temperatur und jährlicher Niederschlag charakterisiert. Die Ergebnisse zeigten, dass sich die 12 Arten in ihrem jahreszeitlichen Reproduktionsmuster unterschieden und dass diese Variation am Besten durch ein Zusammenspiel von phylogenetischen und ökologischen Faktoren erklärt werden konnte. Für die zweite Studie habe ich zwischenartliche Variationen in der sozialen Toleranz an sechs Mausmakiarten untersucht. Hierzu habe ich inter-individuelle Muster von affilitiven und agonistischen Verhaltensweisen sowie soziale Dominanz erfasst, indem ich experimentell zusammengestellte Dyaden in einem standardisierten Begegnungsexperiment beobachtet habe. Die sechs untersuchten Mausmakiarten gehören drei verschiedenen phylogenetischen Clustern an, die zwei Waldhabitate (trochen versus feucht) bewohnen und sich hinsichtlich ihres jahreszeitlichen Reproduktionsmusters (siehe Studie 1) unterscheiden. Sechs Männchen- Weibchen Dyaden und sechs Männchen-Männchen Dyaden wurden in einem standardisierten Begegnungsparadigma für die ersten drei Stunden der Aktivitätsphase an sechs aufeinanderfolgende Tagen beobachtet. Die gemeinsame Nutzung des zur Verfügung stehenden Raumes, die Frequenz des nicht-agonistischen Körperkontakts, die Aggressionsrate und die Anzahl intra-sexueller und inter-sexueller Konflikte wurden quantifiziert und analysiert. Die Ergebnisse zeigen verschiedene Level von sozialer Toleranz in den sechs verschiedenen Arten, die sich durch ein komplexes Zusammenspiel von Waldhabitat und Reproduktionsmuster erklären lassen, wobei der phylogenetische Faktor von geringer Bedeutung ist.

Zusammenfassend, geben die beiden Studien neue Einblicke in die Divergenz der jährlichen Reproduktionsmuster von Microcebus spp., welches die taxonomische Unterteilung der sechs untersuchten Arten unterstützt. Überdies zeigen die Ergebnisse, dass die sechs Arten sich auch im Grad der sozialen Toleranz unterscheiden. Obwohl das jährliche Reproduktionsmuster und die soziale Toleranz von ökologischen Faktoren beeinflusst waren, so war dieser Faktor nicht ausreichend, um die zwischenartlichen Variationen vollständig zu erklären. Stattdessen war ein Zusammenspiel von ökologischen und phylogenetischen Faktoren für das Reproduktionsmuster und zwischen ökologischen und reproduktionsspezifischen Faktoren für die soziale Toleranz wichtig. Folglich deuten die Ergebnisse dieser Doktorarbeit darauf hin, dass die derzeitigen ökologischen Hypothesen nicht ausreichend sind die komplexen Beziehungen zwischen Ökologie, Reproduktion und Aggression in dieser Primatenradiation zu erklären. Weitere Studien sind daher notwendig, welche alle Mausmakiarten und ihr Reproduktionsmuster mit einbeziehen.

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Chapter 1 - General introduction

1.1 Background Madagascar hosts an extraordinary diversity of flora and fauna with unparalleled levels of endemism (Myers et al., 2000). All taxa of the primate infraorder Lemuriformes (lemurs) are 100% endemic to the island of Madagascar. Lemurs are found on a variety of ecosystems in Madagascar: evergreen humid forests in low and mid-altitude, lower montane forests in the eastern and central part, deciduous dry forests and scrubland in the western and southern part of Madagascar. They can even be found in mangroves and marshlands around lakes, rivers or at the seaside (e.g., Andriantompohavana et al., 2006, Du Puy and Moat, 1996, Gardner, 2016, Rasoazanabary, 2004, Roos and Kappeler, 2006). The living lemur taxa are classified into five families: Cheirogaleidae (Gray, 1873), Lepilemuridae (Stephan and Bauchot, 1965), Lemuridae (Gray, 1821), Indriidae (Burnett, 1828) and Daubentoniidae (Gray, 1863). Unfortunately, Madagascar is among one of the two countries with the greatest number of threatened and declining primate species together with Indonesia (Estrada et al., 2018). Most lemur species are classified as threatened according to the IUCN Red List (2018) into categories like vulnerable (VU: 16.66%), endangered (EN: 45.83%) and critically endangered (CR: 12.5%). Their main conservation threats are the severe forest fragmentation and habitat loss (Mittermeier et al., 2006). Under this unfortunate panorama, habitat protection and conservation are essential for the long-term survival of lemurs. Furthermore, understanding and exploring the natural history and ecological requirements of each species are of utmost importance in order to achieve this goal. However, most studies have so far been conducted on the diurnal gregarious species and much less is known about the nocturnal species. The smallest and most cryptic species among lemurs belong to the family Cheirogaleidae. This family is subdivided into five genera: Allocebus (one species), Cheirogaleus (nine species), Microcebus (24 species), Mirza (two species), and Phaner (four species) (Groves, 2000, Hotaling et al., 2016, Kappeler et al., 2005, Louis Jr and Lei, 2016, Markolf et al., 2011, Mittermeier et al., 2010, McLain et al., 2017). The genus Microcebus is exceptional in this family due to its large species diversity and geographical spread, although the animals are difficult to find in nature due to their nocturnal secretive lifestyle. Apart from their taxonomy, datasets on the life history, reproduction, social behavior and ecology are still lacking for many mouse lemur species. This study intends to contribute to filling some of these gaps in knowledge by adding new information on the reproductive schedules and social

1 tolerance (including behavioral correlates and social dominance) of six species of Microcebus.

1.2 Social tolerance and social relationships in primates

Social tolerance coordinates social relationship and predominantly affects the pattern of affiliation and agonism in gregarious primates (Ciani et al., 2012, Kappeler and van Schaik, 2002). Fichtel and colleagues (2017) presented two approaches to characterize social tolerance: the first approach evaluates the behavioral correlates of social tolerance such as social contact, allogrooming and proximity, whereas the second approach assesses the outcomes of social tolerance, for example, aggression rates or conflicts in a potentially competitive context such as in a co-feeding task.

In diurnal group-living mammals including non-human primates, social relationships are based on the costs and benefits resulting from direct or indirect forms of competition and cooperation between individuals. For example, frequent direct contest competition typically leads to the establishment of a stable hierarchy system within groups (Scott, 1992). Group living and cooperation has often been reported to be beneficial in the context of predator avoidance (van Schaik, 1983), for defending territories, shelter, food resources or water (Wrangham, 1980). Social relationships are typically characterized by the specific patterns of affiliative and aggressive behaviors (Rowell, 1974).

1.2.1 Affiliation

Affiliative behavior is observed between two individuals or subgroups of individuals and comprises all socio-positive interactions, for example, huddling or allogrooming (Puga- Gonzalez et al., 2009). In diurnal primates such as New World and Old World monkeys and apes, social interactions are to a large extent characterized by affiliation (Sussman et al., 2005). Consequently, in stable groups, several forms of cooperative benefits can be obtained by affiliative interactions such as social bonds, coalition formation and reconciliation after conflicts. These behavioral patterns facilitate cooperation but also help to avoid costly aggression (Sussman et al., 2005). One prominent affiliative behavior, allogrooming, conveys several functions, for instance, cleaning fur so that lemurs keep themselves free of ectoparasites and intensifying social bonds (Barton, 1985). It is also regarded as a mechanism of exchange and reciprocity (Henzi et al., 2003), for instance, during reconciliation after a 2 fight between two dyad partners (Arnold and Aureli, 2007), and helps to decrease anxiety, tension and stress (Goosen, 1987, Sclafani et al., 2012).

1.2.2 Agonistic behavior

Empirical data on agonism showed that it has a much lower frequency than affiliation and other behaviors. The mean rate of agonism is reported to be approximately 0.60 events per hour in monkeys and 0.09 per hour in apes (Sussman et al., 2005). Previous studies reported that agonistic interactions represented less than 1% of all social behaviors of diurnal lemurs (Sussman et al., 2005), which are displayed between two or more individuals within the group. As resources (food or water) are very often restricted in supply, members of the same social group often compete with each other for access to them (De Waal and Luttrell, 1989). Contest and scramble competition are the predominant competition regimes and depend on resource quality and distribution (Isbell, 1991, van Schaik, 1989). In the context of feeding competition, agonism is expected to be extensive and relatively common among conspecifics (van Schaik and van Hooff, 1983, Wrangham, 1980). Apart from that, defending territories results in agonistic interactions between different groups (Wrangham and Peterson, 1996). Another agonistic context is competition between two or more males in order to gain access to receptive females during certain periods (Mason and Mendoza, 1993). However, the use of agonistic behaviors may also be detrimental to the health (e.g., wounds), and individuals should engage in physical conflicts only if the benefits (e.g., gaining access to resources) are greater than the costs (De Waal and Luttrell, 1989). Whenever individuals repeatedly compete directly, it may be therefore beneficial to establish formal dominance hierarchies, by which open day-to-day conflicts can be avoided. Such a dominance hierarchy can coincide with the evolution of formalized submissive behaviors and can establish some pattern of social tolerance between group members as long as differential access to resources is maintained (De Waal and Luttrell, 1989).

1.3 The evolution of social dominance In many species of fish, amphibians, reptiles, and birds, adult females can be of larger body size than males (Coddington et al., 1997, Darwin, 1874, Ralls, 1976). In contrast, mammalian males are often larger and physically stronger compared to females, due to the morphological adaptations to fight such as physical strength, large canine teeth, horns or antlers (Darwin, 1871, Jolly, 1984). The evolution of these sexually dimorphic weapons and

3 corresponding high aggression levels is explained by high intraspecific sexual competition between mammalian males, which often form harem systems with several females for mating. As a consequence, dominance among males has repeatedly been shown to correlate with reproductive success (Cowlishaw and Dunbar, 1991, Wroblewski et al., 2009).

1.4 The evolution of social tolerance and female dominance

According to De Waal (1989) social tolerance is defined as “Low competitive tendency, especially by dominants towards subordinates”. Therefore, social tolerance determines individual behavior within dyads or conspecifics in relation to proximity. Species showing high social tolerance also have a higher social plasticity (Fichtel et al., 2017). For instance, individuals do not have difficulty living within the band (Lonsdorf et al., 2009), have increased prosocial and cooperation behavior (Burkart et al., 2014, Hare et al., 2007), or can easily become familiar with intruders (Tan and Hare, 2013). Intrasexual or intersexual levels of proximity represent well the degree of social tolerance within groups and species, which also influences the frequency of agonistic conflicts and the establishment of social dominance (McCort and Graves, 1982, Rioja-Lang et al., 2009).

Dominance hierarchies are based on dyadic relationships between dominant and subordinate individuals in a social group (Drews, 1993). Dominance style in primate societies, like in rhesus macaques, for instance, ranges from egalitarian to despotic individuals (De Waal and Luttrell, 1989, Dubuc et al., 2012). Female dominance is defined as the ability of all adult females to consistently evoke submissive behavior in all adult males (Kappeler, 1993) and is very rare in mammals in general (Hrdy, 1981, Jolly et al., 1982, Kappeler, 1993, Ralls, 1976). In lemurs, however, female dominance appears to be the rule rather than the exception and a large amount of literature has accumulated on this particular trait (see Table 1.1). Despite several tests on the role of internal and external factors (Dunham, 2008, Eichmueller et al., 2013, Jolly, 1984, Petty and Drea, 2015), the drivers of the evolution of female dominance in lemurs are still controversially debated (Eichmueller et al., 2013, Ramanankirahina et al., 2011). Previous studies proposed different explanations for the aggressive superiority of female lemurs over males, although most of them focus on some form of energetic constraints that female lemurs are confronted with (e.g., Dunham, 2008, Jolly, 1984, Wright, 1999, Young et al., 1990).

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In general, three types of female dominance are described: 1) Unambiguous female dominance: all females are dominant over all males, as documented in Eulemur macaco flavifrons (Digby and Mclean Stevens, 2007, Digby and Kahlenberg, 2002); Propithecus diadema edwardsi (Pochron et al., 2003); Microcebus murinus (Radespiel and Zimmermann, 2001); Microcebus griseorufus (Génin, 2013); Microcebus berthae (Dammhahn and Kappeler, 2005). 2) Moderate female dominance: conflicts are less often decided, but females win significantly more conflicts than males, such as in Phaner furcifer (Schülke and Kappeler, 2003) or Microcebus lehilahytsara (Hohenbrink et al., 2016). 3) Female feeding priority: dominance is restricted to the feeding context as in Propithecus coquereli (Kubzdela et al., 1992, Richard and Heimbuch, 1975) and Eulemur mangoz (Curtis and Zaramody, 1999). Female dominance can also be absent in some species of lemurs, for instance, in Microcebus ravelobensis and Eulemur sp. (Table 1.1) (Eichmueller et al., 2013, Pereira et al., 1990, Pereira and McGlynn, 1997).

Table 1.1: Distribution of different types of female dominance among lemur Type Species family Reference Microcebus murinus Cheirogalidae (1), (2) Microcebus griseorufus Cheirogalidae (2) Microcebus berthae Cheirogalidae (3) Lemur catta Lemuridae (4), (5) Varecia variegata variegata Lemuridae (6), (7) Unambiguous female dominance Varecie variegata rubra Lemuridae (7), (8) Eulemur macaco flavifrons Lemuridae (9), (10) Indri indri Indridae (11) Propithecus diadema edwardsi Indridae (12) Propithecus tattersalli Indridae (13) Avahi occidentalis Indridae (14) Microcebus lehilahytsara Cheirogalidae (15) Microcebus murinus Cheirogalidae (15) Phaner furcifer Cheirogalidae (16) Eulemur macaco Lemuridae (17) Eulemur rubriventer Lemuridae (18) Moderate female dominance Eulemur coronatus Lemuridae (5), (18) Hapalemur griseus griseus Lemuridae (10)

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Propithecus coronatus Indridae (19) Daubentonia madagascariensis Daubentonidae (20) Eulemur mangoz Lemuridae (21) Female feeding priority Hapalemur griseus alaotrensis Lemuridae (22), (23) Propithecus verrauxi Indridae (24) Propithecus coquereli Indridae (24), (25) Microcebus ravelobensis Cheirogalidae (26) Eulemur fulvus rufus Lemuridae (5), (27) No female dominance Eulemur fulvus mayottensis Lemuridae (28) Eulemur fulvus sanfordi Lemuridae In (29) (30) Eulemur fulvus collaris Lemuridae (30) (1) Radespiel and Zimmermann (2001), (2) Génin (2013), (3) Dammhahn and Kappeler (2005), (4) Kappeler (1990), (5) Pereira et al. (1990), (6) Kaufman (1991), (7) Raps and White (1995), (8) Meyer et al. (1999), (9) Digby and Kahlenberg (2002), (10) Digby and Mclean Stevens (2007), (11) Pollock (1979), (12) Pochron et al. (2003), (13) Meyers (1995a), (14) Ramanankirahina et al. (2011), (15) Hohenbrink et al. (2016), (16) Schülke and Kappeler (2003), (17) Fornasieri et al. (1993), (18) Marolf et al. (2007), (19) Ramanamisata et al. (2014), (20) Rendall (1993), (21) Curtis and Zaramody (1999), (22) Mutschler et al. (2000), (23) Waeber and Hemelrijk (2003), (24) Richard and Heimbuch (1975), (25) Kubzdela et al. (1992), (26) Eichmueller et al. (2013), (27) Pereira and McGlynn (1997), (28) Roeder and Fornasieri (1995), (29) Erhart and Overdorff (2008), (30) DelBarco-Trillo et al. (2012)

1.5 Mouse lemurs (Microcebus spp.)

Malagasy mouse lemurs (Cheirogaleidae) are regarded as being a very suitable model for studying the evolution of sociality in primates since they share a combination of rather basal traits among lemurs (e.g., small body size, solitary foraging habits, and nocturnality), but already form individualized social relationships with members of their sleeping groups (Cowlishaw and Dunbar, 2000, Kessler et al., 2016, Martin, 2000). The genus Microcebus comprises the smallest living primates with a body mass between 30g to 80g. Females can have 1-3 infants per litter once or twice a year following a very brief receptive period and about 60 days of pregnancy. Infants are raised in a tree hole or nest during the first weeks of life (Ross, 2001, Schwab, 2000). Mouse lemurs have an omnivorous diet and use variable

6 types of substrates as shelters during their daily resting period (Corbin and Schmid, 1995, Eichmueller et al., 2013, Hladik et al., 1980, Kappeler and Rasoloarison, 2003, Martin, 1973, Radespiel et al., 2003, Weidt et al., 2004).

Microcebus population densities are high throughout Madagascar, but Setash et al., in (2017) discovered that population densities in the western dry forests seem to be higher than in the eastern humid forests. Females of several species form stable sleeping groups consisting of two to nine related members, and their coordinated space use is probably governed by acoustic and olfactory signals (Braune et al., 2005, Charles-Dominique, 1978, Pagès-Feuillade, 1988, Radespiel, 2000a, Radespiel et al., 1998, Radespiel and Zimmermann, 2001, Wimmer et al., 2002). Males, on the other hand, can either sleep alone or form sleeping groups with other males or females (Radespiel et al., 1998, Schmelting, 2000). Females and males establish non-exclusive home-ranges, with co-sleepers having higher home-range overlaps than non-co-sleepers (Eberle and Kappeler, 2006, Jürges et al., 2013, Lutermann et al., 2006). Mouse lemurs are typically categorized as living in a dispersed multi-male/multi- female neighborhood system (Kappeler and Rasoloarison, 2003, Mittermeier et al., 2006, Radespiel, 2000b, Weidt et al., 2004). The mating system has been categorized as being promiscuous with a considerable amount of intrasexual competition among males for gaining access to estrous females and some level of female choice (Craul et al., 2004, Crofoot, 2012, Eberle and Kappeler, 2004a, Eberle and Kappeler, 2004b, Radespiel et al., 2001, Radespiel and Zimmermann, 2003, Schmelting, 2000).

For a long time, Microcebus was merely divided into two species and distinguished by fur coloration: the reddish form from the eastern clade (Microcebus rufus) and the grayish form from the western clade (Microcebus murinus) (Pastorini et al., 2001, Rasoloarison et al., 2000, Yoder et al., 2002, Yoder et al., 2000). Subsequent studies have broadened our view by focusing on the phylogeny and taxonomy of this genus and have led to numerous species descriptions over the last 20 years (Andriantompohavana et al., 2006, Louis Jr et al., 2006, Louis Jr et al., 2008, Olivieri et al., 2007, Radespiel et al., 2008, Radespiel et al., 2012, Rasoloarison et al., 2000, Rasoloarison et al., 2013, Yoder et al., 2000, Zimmermann et al., 1998). The species count within Microcebus spp. has reached 24 described species so far which are mostly distributed sparsely across the island (Figure 1.1, Hotaling et al., 2016, Yoder and Nowak, 2006).

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Figure 1.1 Distribution map for Microcebus spp. throughout Madagascar`s geographical ranges are highlighted in color or shown as dashed lines (changed after Radespiel, 2006)

A recent study on mouse lemurs revealed that female dominance varies seasonally in its expression and seems to be variable within the genus Microcebus (Hohenbrink et al., 2016, Table 1.1). However, so far, only three species have been studied under natural conditions (M. ravelobensis, M. griseorufus and M. berthae), one species (M. murinus) being studied both under natural conditions and in captivity, and M. lehilahytsara having only been studied in captive and semi-captive populations (Dammhahn and Kappeler, 2005, Eichmueller et al., 2013, Génin, 2013, Hohenbrink et al., 2016, Jürges et al., 2013, Radespiel and Zimmermann, 2001). Most authors assume a relationship between female dominance and some aspects of 8 female reproductive activity in a seasonally challenging environment that might limit reproduction (i.e., high fluctuations and unpredictability in temperature and rainfall) (Dunham, 2008, Gould and Sauther, 2007, Hohenbrink et al., 2016, Jolly, 1984). Only five out of 24 mouse lemur species have been studied so far with respect to the extent and nature of female dominance (Table 1.1).

Six species (Microcebus myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi, M. margotmarshae and M. mamiratra) were selected for this study in order to provide relevant information on their reproductive schedules and their social behavior, including their tendency to establish social dominance when meeting with conspecifics on a regular basis (Figure 1.2). These six species are found in a region covering seven Inter-River Systems (IRS) ranging from western to northwestern Madagascar (Figure 1.1). They are briefly described below and arranged in the order from the west to the north (Olivieri et al., 2007).

Figure 1.2 Pictures of the six Microcebus species studied. All photographs taken by the author.

The Pygmy mouse lemur, Microcebus myoxinus (Rasoloarison et al., 2000, Yoder et al., 2000), is found between the Betsiboka River and the southern Tsiribihina River, inhabiting dry deciduous forests. This species prevails in the forests of Belo sur Tsiribihina, heavily degraded deciduous forests of Aboalimena, in the Tsingy of the Bemaraha National Park and Nature Reserve, and in the Tsingy of the Namoroka National Park (Mittermeier et 9 al., 2008, Rasoloarison et al., 2000). They also have been recorded in the mangroves of Baie de Baly which is near Antsakoamarovitiky (Hawkins et al., 1998). Knowledge about reproduction, socio-ecology, social behavior and their vocal repertoire is still lacking.

The golden-brown mouse lemur, Microcebus ravelobensis (Zimmermann et al., 1998) is found within one inter-river system (IRS Ia) located between the Betsiboka River and the Mahajamba River, in dry deciduous forest habitats. This species is found throughout the Ankarafantsika National Park (Rakotondravony and Radespiel, 2009, Rendigs et al., 2003) and was first found in the vicinity of Lac Ravelobe from which its scientific name is derived (Zimmermann et al., 1998). However, it can be found as well in the dry deciduous forests of Mariarano Classified Forest (Mittermeier et al., 2008, Olivieri et al., 2007) and other smaller forest fragments in the same inter-river system (Guschanski et al., 2005, Olivieri et al., 2007, Steffens and Lehman, 2018). M. ravelobensis is omnivorous (Radespiel et al., 2006, Thorén et al., 2011). M. ravelobensis lives in a dispersed multi-male/multi-female system and forms stable sleeping groups composed of related males and females that sleep in various substrates or also build nests themselves (Radespiel et al., 2003, Radespiel et al., 2009, Thorén et al., 2010, Weidt et al., 2004). Individuals communicate via acoustic and olfactory signals to signal group ownership and to coordinate group reunions (Braune et al. 2005). M. ravelobensis lives sympatrically with M. murinus (Zimmermann et al., 1998) in many but not all sites (Rakotondravony and Radespiel, 2009). Reproduction is seasonal and occurs from August to November (Randrianambinina et al., 2003). The onset of reproduction starts one month earlier compared to M. murinus (Randrianambinina et al., 2003, Schmelting et al., 2000).

The Bongolava mouse lemur, Microcebus bongolavensis (Olivieri et al., 2007), situated between Mahajamba and Sofia River in northwestern Madagascar, dwelling in dry deciduous forest habitats. This species is so far known from four sites consisting of three small forest fragments (Ambodimahabibo, Mahajamba-Est and Maroakata) and Marosely is the only larger forest fragment of dry deciduous forest (Olivieri et al., 2007, Randrianambinina et al., 2003). Microcebus bongolavensis live in partial sympatry with M. murinus. Knowledge about reproduction, socio-ecology, social behavior and their vocal repertoire is still lacking.

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The Danfoss's mouse lemur, Microcebus danfossi (Olivieri et al., 2007), is found in one inter-river system (IRS III) situated between the Sofia and Maevarano River in northwestern of Madagascar. M. danfossi is found in four different forest states: nine forest fragments (Ambongabe, Antonibe, Antanambato, Andranotsara, Ankaramikely, Ambararata, Beanamalaho, Betsatsika, Mahatsinjo), one “Station Forestière” (Anjiamangirana) managed by the MAF “ Madagascar Aye aye Found”, one “Special Reserve“ (Bora) and in four protect zones located in northwestern Madagascar (Marosakoa, Anjajavy, Ambarijeby and Bekofafa) (Mittermeier et al., 2010, Olivieri et al., 2005, Olivieri et al., 2007, Randrianambinina et al., 2010). Knowledge about reproduction, socio-ecology, social behavior and their vocal repertoire is still lacking.

Margot Marsh's mouse lemur, Microcebus margotmarshae (Louis Jr et al., 2008), seems to be the most sparsely distributed (IRS V) of all studied species, limited to the Andranomalaza river to the south and Sambirano River to the North (Louis Jr et al., 2008; Rina Evasoa and Zimmermann, unpubl. data). M. margotmarshae is so far only known to be found in low altitude evergreen humid forests. This species was first described as being in the Antafondro Classified Forest (Andriantompohavana et al., 2006, Louis Jr et al., 2008). Knowledge about reproduction, socio-ecology, social behavior and their vocal repertoire is still lacking.

Claire's mouse lemur, Microcebus mamiratra (Andriantompohavana et al., 2006), prevails in one inter-river system (IRS VI) in addition to the island of Nosy Bé, where it was first described (Andriantompohavana et al., 2006). There, it is mainly found in the Lokobe Strict Nature Reserve and inhabits low altitude evergreen humid forests (Du Puy and Moat, 1996). Vocal communication has been studied recently (Hasiniaina et al., 2018) but knowledge about reproduction, socio-ecology and social behavior is still lacking.

1.6 Anthropogenic pressures and threats effecting mouse lemur populations and species Human population growth in Madagascar is leading to a continuous loss of lemur habitat and population decline (Crist et al., 2017). The six species of Microcebus selected for this study are threatened by various human activities: humans are extending anthropogenic pressures by continuous deforestation caused by slash and burn agriculture and seasonal bushfires as well as bush-hunting for food, even opportunistically for mouse lemurs

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(Mittermeier et al., 2010). Therefore, Microcebus habitats are declining in quantity and quality and are being severely fragmented (Olivieri et al., 2008). Besides humans, numerous other predators also prey on mouse lemurs, for instance, the nocturnal long-eared owl (Asio madagascariensis), the barn owl (Tyto alba) and the diurnal Henst’s goshawk (Accipiter henstii); the colubrid snake (Ithycyphys miniatus), Madagascar tree boa (Sanzinia madagascariensis) and Madagascar ground boa (Acantrophis madagascariensis); the viverid fossa (Cryptoprocta ferox) and the feral narrow-striped mongoose (Mungotictis decemlineata) (Goodman, 2003, Rahlfs and Fichtel, 2010, Rasoloarison et al., 1995). None of the six Microcebus species have been kept in captivity so far, except for four individuals of M. mamiratra kept in the “Parc Botanique et Zoologique de Tsimbazaza”, Antananarivo Madagascar (Mittermeier et al., 2008). Owing to the criteria stated above, all six study species are considered as being threatened by extinction in the wild (IUCN, 2018). M. ravelobensis, M. bongolavensis, M. danfossi, M. margothmarshae and M. mamiratra are assessed as Endangered (EN), while M. myoxinus is categoried as Vulnerable (VU).

1.7 Aims and hypotheses

A central and controversially debated topic in behavioral biology is how and why social dominance evolves during the evolution in primates and how the evolution of female dominance in lemurs can be explained, as it contrasts to the typical patterns of male dominance in other primate radiations. Comparatively few studies have investigated social dominance in nocturnal strepsirrhines so far (listed in Table 1.1). Most lemur studies suggest that some reproductive or energetic constraint in female lemurs may best explain the evolution and/or maintenance of female dominance in this clade. Nevertheless, both reproductive and behavioral data are still missing for many of the recently described nocturnal taxa.

The general aim of my thesis is to investigate the interspecific variation of reproductive schedules and their relationship to the variation in intra-sexual and inter-sexual interactions in six closely related species of mouse lemurs (Microcebus myoxinus, M. lehilahytsara, M. mamiratra, M. margotmarshae, M. ravelobensis, M. bongolavensis and M. danfossi). The following specific questions will be addressed:

12 i. Is there any variation in reproductive schedules among the targeted mouse lemur species in Madagascar? Does a relationship occur between reproductive schedules, phylogenetic relationships and ecology? ii. How does social tolerance, and its outcomes vary among the six studied mouse lemur species under a standardized experimental social encounter paradigm? Can social tolerance and its outcomes be predicted by phylogenetic relationships, ecology and reproductive activity differences among the study species?

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Chapter 2 - Variation in reproduction of the smallest‐bodied primate radiation, the mouse lemurs (Microcebus spp.): A synopsis

Published in 2018 in the journal American Journal of Primatology. Volume 80 issue 7 (DOI: 10.1002/ajp.22874) by

Mamy Rina Evasoa1, Ute Radespiel1, Alida Frankline Hasiniaina1, Solofonirina Rasoloharijaona2, Blanchard Randrianambinina2, Romule Rakotondravony2, Elke Zimmermann1

1Institute of Zoology, University of Veterinary Medicine, Hannover, Germany

2Faculty of Sciences, University of Mahajanga, Madagascar

Reproduction is a fundamental trait in the life history of any species and contributes to species diversity and evolution. Here, we aim to review the barely known variation in reproductive patterns of the smallest-bodied primate radiation, the Malagasy mouse lemurs, focusing on twelve species of four phylogenetic clades. We present a new reproductive field dataset collected between May and November 1996–2016 for nine species (Microcebus murinus, M. myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi, M. sambiranensis, M. margothmarshae, M. mamiratra, and M. lehilahytsara) and add published field information on three additional species. In the majority of species, the estrus of females was recorded in the period of long days (day length longer than 12 hr), whereas male testes size increased about one to three months prior to this. Reproductive schedules varied considerably between the four clades. Sympatric species-pairs of different clades differed in the timing of female and male reproduction, suggesting strong phylogenetic constraints. Populations of the same species in a different ecological setting varied in the onset of reproduction, suggesting substantial environmental plasticity. Warm temperatures and rainfall throughout the year may allow for less expressed reproductive seasonality. Our results suggest that an interplay between phylogenetic relatedness, ambient temperature (as a proxy for thermos regulatory constraints), and rainfall (as a proxy for food availability), may best explain this variation. Findings further point to a more complex control of mouse lemur reproduction than previously described and illuminate phylogenetic constraints and adaptive potentials in behavioral reaction norms of a species-rich primate radiation.

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Chapter 3 – Determinants of interspecific variation in social tolerance in mouse lemurs (Microcebus spp.) Submitted to BMC Ecology by

Mamy Rina Evasoa1, Elke Zimmermann1, Alida Frankline Hasiniaina1, Solofonirina Rasoloharijaona2, Blanchard Randrianambinina2, Ute Radespiel1

1Institute of Zoology, University of Veterinary Medicine, Hannover, Germany

2Faculty of Sciences, University of Mahajanga, Madagascar

Background: Social tolerance strongly influences the patterns of affiliation and aggression in animal societies. However, not much is known about the variation of social tolerance in species living in dispersed social systems that combine solitary foraging activities with the need of coordinating social interactions with co-sleepers or neighbors on a regular basis. This study aims to investigate for the first time the sources of variation in social tolerance (assessed by inter-individual patterns of affiliation) and by its outcomes (agonism and social dominance) within a Malagasy primate radiation with dispersed social systems, the mouse lemurs. Six mouse lemur species are selected as model species that belong to three different taxonomic clades, live in two types of forest environments (dry and humid), and differ with respect to reproductive activity. Six male-female and six male-male dyads of each species were tested temporarily in an standardized social encounter paradigm in Madagascar to collect data on joint use of space, non-agonistic body contacts, aggression rates, the number of conflicts and the establishment of intra- and intersexual dominance. Results: Male-female dyads of the six species differed significantly in their degree of social tolerance and agonism. In contrast, the variations between male-male dyads could not be explained by one parameter only, but clade membership, forest type, reproductive state as well as species were all suggested to be partially influential. Only one species (M. mamiratra) showed signals of unambiguous female dominance in all male-female dyads, whereas the others showed no or moderate female dominance. Conclusions: Variations in social tolerance and its outcomes are most likely the result of an interaction of forest type and reproductive activity and only to a lesser extent of clade membership. The study suggests that species inhabiting the dry forests may be energetically constrained during the resource-poor dry season and may consequently show lower levels of aggression. In addition, species with reproductively active females have higher aggression rates and more agonistic conflicts, if they are not energetically constrained. The study 15 confirms a high degree of social plasticity in these small solitary foragers that supports their taxonomic distinctiveness and requires further scientific attention.

Keywords: Microcebus myoxinus, Microcebus ravelobensis, Microcebus bongolavensis, Microcebus danfossi, Microcebus margotmarshae, Microcebus mamiratra, affiliation, female dominance, aggression, Madagascar

3.1 Introduction

Social relationships are generally described through patterns of social interactions between individuals and form the central element of the social structure of species [1]. Social relationships are governed by variable degrees of social tolerance that strongly influence the patterns of affiliation and aggression that can be observed between individuals [2-4]. Accordingly, de Waal and Luttrell [5] defined a high social tolerance as “low competitive tendency, especially by dominants towards subordinates”. Variations in social tolerance can decide on various fitness-relevant parameters such as access to resources [5] or the selectivity and intensity of cooperation with conspecifics [6, 7]. Social tolerance levels in non-human primates have been described to differ largely between tolerant/egalitarian to intolerant/despotic societies and much attention has already been given to this categorization, for example, in various diurnal group-living primates such as macaques [5, 8]. However, many species of primates do not live in cohesive social groups, but form dispersed social systems that are based on solitary foraging activities, but may include the formation of stable sleeping groups during periods of inactivity [9-14]. Within these systems, social interactions still occur on a regular basis, since these species are only rarely strictly territorial and therefore do meet conspecifics regularly within their home range. During such encounters, a certain level of social tolerance should be advantageous, as solitary foragers also need to coordinate various activities, such as mating [15-18], sleeping group reunions [19], access to resources when meeting at a food source that may or may not be monopolized [3, 20], coordinated movements or space use [19, 21] or predator avoidance [22]. Despite its importance, social tolerance is much less studied in small nocturnal solitary foragers due to their small size, nocturnal activity pattern and the associated difficulty to observe social encounters in dense forest environments [12]. Fichtel et al. [3] recently discriminated between two different approaches to study social tolerance: the first investigates the behavioral correlates of social tolerance (e.g., social

16 contacts, allogrooming, proximity), whereas the second approach quantifies the outcomes of social tolerance, such as co-feeding behavior and aggression rates, within an experimentally induced competitive situation. The study presented here is combining both approaches in a single design by studying for the first time the correlates (i.e. patterns of affiliation) AND the outcomes of social tolerance (i.e. agonism and social dominance) with a standardized experimental social encounter paradigm [23-25] that is applied with a comparative perspective to six species within a single primate radiation, mouse lemurs (Microcebus spp.). For five of these species, there is so far no information available on social structure, neither on its components, social interactions and relationships, nor on social tolerance and social dominance. Mouse lemurs are nocturnal lemurs and endemic to the various humid and dry forest habitats of Madagascar [26]. A total of 24 mouse lemur species have so far been described [27]. The social system of many of these species has not yet been studied, and current knowledge is largely based on the study of seven species only (M. murinus, M. ravelobensis, M. berthae, M. griseorufus, M. lehilahytsara, M. rufus, M. sambiranensis), most of which form some kind of sleeping groups (male-male, male-female, or female-female) during daytime in a shelter at least temporarily, and have non-exclusive, largely overlapping home ranges not only with members of the same sleeping group but also with male strangers [reviewed in 11, 13, 28, 29]. However, based on extensive nocturnal survey work that has been conducted in many locations across Madagascar, it is evident that probably all mouse lemur species live in dispersed neighborhood systems [30], as it is typically single individuals and not groups that are encountered during the night [31-34]. It is also known that mouse lemur reproduction is highly seasonal in most species with the likely exception of those that inhabit warm lowland evergreen rainforests with high productivity such as those occurring some northern parts of Madagascar, e.g. in the region of Nosy Bé [35]. Not much is known about the social relationships in these dispersed social networks. However, recent work from captivity suggests that female dominance that is untypical for mammals but formerly thought to be typical for most lemur species [36, 37], may be much more variable and plastic in mouse lemurs than expected [23, 24, 38]. For example, conflict rates, the probability for females to win conflicts, and the number of dominant females varied between species (M. murinus, M. lehilahytsara) and season (reproductive vs. non-reproductive) and furthermore depended on age and breeding experience [24, 38]. All of these variables can be categorized as outcomes of social tolerance (see above). Whether this diverse, plastic and complex behavioral

17 phenomenon is the outcome of adaptive evolutionary trajectories of different species [24, 39] or resulted from phylogenetic constraints [36], could not be clarified so far. The aim of this study is to study the variation in social tolerance (i.e., patterns of affiliation) and its consequences (i.e., agonism and social dominance) among six mouse lemur species (M. myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi, M. margotmarshae, M. mamiratra) that have allopatric distributions along a geographic transect from northwestern to northern Madagascar (Figure 3.7). These six species fall into three different phylogenetic clades with M. mamiratra and M. margotmarshae belonging to one clade (clade 1), M. ravelobensis, M. bongolavensis and M. danfossi forming a separate clade (clade 2), and M. myoxinus belonging to another clade (clade 3, Table 3.4, [27, 40]). If social tolerance is mainly influenced by phylogenetic constraints, it can be predicted that members of the same clade should show more similarities in social tolerance (i.e., affiliation) and its outcomes (i.e., agonism and social dominance) than members of different phylogenetic clades. The six species occur in two contrasting forest types, dry deciduous forests (M. myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi) and low altitude humid forests (M. margotmarshae, M. mamiratra), that differ largely in the amount of yearly rainfall and the seasonality in precipitation [35]. Since rainfall has been shown to correspond to forest productivity [41, 42], it can be predicted that strong seasonal resource shortage in dry forests may constrain social tolerance of mouse lemurs in those areas more than of species inhabiting humid forests. It can therefore be expected that the two species living in humid forests (M. margotmarshae, M. mamiratra) should show higher affiliation, less signs of aggression and less expressed dominance than species living in the dry deciduous forest. All species were studied in the dry season between May and October. However, not all of them were studied during the same reproductive period, since no information was available on reproduction of five of the six species at the beginning of this study. Our work then revealed that females of three species showed signals of reproductive activity (M. danfossi, M. margotmarshae, M. mamiratra), whereas females of the three other species showed no signal of reproduction [35]. As it is known from M. murinus that (1) conflict rates and female dominance vary between reproductive and non-reproductive season [24], and that (2) males compete strongly for the access to estrous females during the reproductive season [15], it is predicted that social tolerance (i.e. affiliation) should be lower and accordingly its outcomes (i.e. aggression rates) should be higher within and between sexes when estrous females are present in the population or in a dyad.

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This study will compare the relative influence of phylogeny, forest type and reproductive activity on social tolerance (i.e., patterns of affiliation) and its outcomes (i.e., agonism and social dominance) in six male-male and six male-female dyads of six mouse lemur species, respectively, that were tested with a standardized social encounter paradigm [23-25]. Female-female dyads were not tested, because under natural condition their social behavior is mainly directed at related members of the same sleeping group [11, 43-45] and can therefore not be not well evaluated with this paradigm. Model quality is evaluated against a null model (no fixed factor) and against a simple model of pure species differences that are not connected to phylogeny, forest type or reproductive activity. 3.2 Results 3.2.1 Variation of affiliation during the encounters among dyad types and species The joint stay in the sleeping box, the joint use of a cage compartment, the number of total body contacts and the number of co-feeding events were analyzed to evaluate systematic variations in affiliation between dyad partners and species. Dyads stayed together in the sleeping box in 5.7 – 214.7 intervals per observation hour (one observation hour = 240 intervals), i.e. during 2.4% – 89.5% of all possible intervals. The species model (#2) was significantly better than base model 0 (#1) at explaining the variation in the dataset, indicating that species differed significantly in the frequency of staying together in the sleeping box (Fig. 3.1, Table 3.5, Test 1). Although the forest model (#3), the clade model (#4), and the reproduction model (#5) each performed significantly better than model 0 (Table 3.5, Test 1), none of them performed as well as the species model (#2, Table 3.5, Test 2).

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Figure 3.1 Species comparison of the joint use of sleeping box (interval frequency/observationhour). Mean, box: standard deviation, whiskers: minimum, maximum

The subsequent addition of the variable pair type did not improve the species model (#6, Table 3.5). M. myoxinus stayed longest together in the sleeping box and the posthoc test revealed significantly higher rates (median = 159.1 intervals/hr, min = 112.2, max = 189.1) than in M. bongolavensis, M. margotmarshae and M. mamiratra. In contrast, M. mamiratra stayed shortest together in the sleeping box (median = 58.8 intervals/hr, min = 5.7, max = 118.0) and had significantly lower rates than M. myoxinus, M. ravelobensis and M. danfossi (Fig. 3.1, Table 3.5). Pair partners stayed together in the same cage compartment in between 21.8 – 192.2 intervals/hr that both partners spent outside the sleeping box. Joint space use differed again significantly between species, although in this case only the species model (#2) explained significantly more variation than model 0 (Table 3.6, Test 1) and fitted significantly better than the forest, clade, and repro models (#3, #4, #5), respectively (Table 3.6, Test 2). The addition of the variable pair type improved the model fit significantly (Table 3.6, #6), suggesting that male-female dyads and male-male-dyads differed in their joint space use

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(Figure 3.2). As a result, both datasets (mm-dyads, mf-dyads) were analyzed separately in a second step. The joint space use of male-female dyads was best explained by the species model (#8), which was the only significant model among all (#8-11, Table 3.6, Test 1) and fitted significantly better than the forest, clade, and repro model (#8-11, Table 3.6, Test 2). Male- female dyads of M. bongolavensis stayed most frequently together in the same compartment (median = 138.6 intervals/hr, min = 73.2, max = 184.6, Fig. 3.4), which accounted on average for more than half of the intervals (57.8%) that both dyad partners spent outside the box. A posthoc test revealed a significant difference to M. danfossi with the smallest median of 38.0 intervals/hr (min = 9.6, max = 81.4) which accounted on average for only 15.8% of the intervals outside the box. None of the other comparisons were significant. The variations in joint space use of male-male dyads could not be best explained with one single model, i.e., the species, forest or clade model (#13-15) had all very similar AIC and BIC values (Table 3.6, Test 1). Qualitatively, mm-dyads of M. margotmarshae and M. mamiratra showed the highest average rates of joint space use, whereas M. danfossi had the lowest rates as in the mf-dyads (Figure 3.2). The details of the three models and the posthoc test for the species model revealed that (1) M. margotmarshae had significantly higher rates of joint space use than M. ravelobensis, M. bongolavensis and M. danfossi, (2) species living in humid forest had higher rates than species living in dry forest, and (3) species of the northwestern clade had significantly lower rates of joint space use than species from the northern clade (Table 3.6).

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Figure 3.2 Species comparison of joint space use per dyad type (interval frequency/hr both outside box). Mean, box: standard deviation, whiskers: minimum, maximum

The dyads spent between zero and 127.7 intervals per hour outside the sleeping box in physical contact with each other. These variations could not be statistically explained by any single parameter model (Table 3.7, Test 1), neither the species, forest, clade nor the repro model. However, when adding pair type to the species model (#6), it fitted significantly better than the null model (Table 3.7, Test 2, Fig. 3.3). As in the case of joint space use, the total body contacts in mf-dyads could be best explained by the species model (Table 3.7, #8), although post hoc tests only revealed two statistical trends for differences between M. bongolavensis versus M. myoxinus and M. margotmarshae which had lower values, respectively (Figure 3.3). In the case of mm-dyads, the forest model (#14) and the clade model (#15) explained the variation better than the null model (#12, Table 3.7) and they performed equally well, indicating that (1) mm-dyads from the humid forest had more body contacts than those from the dry forest, and (2) mm-dyads from the northwestern clade had significantly less body contacts than those from the northern clade (Table 3.7, Test 2).

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Figure 3.3 Species comparison of total body contact per dyad type (interval frequency/hr both outside box). Mean, box: standard deviation, whiskers: minimum, maximum

Overall, the results on total body contacts largely correspond to the findings on the joint space use, and both variables indeed correlated significantly with each other (Spearman Rank correlation test, rS = 0.572. n = 71, p < 0.0001). In contrast, neither of these two variables correlated significantly with the joint use of the sleeping box (rS-joint space use = -0.1032, n = 71, p = 0.3917, rS-total body contact = -0.1750, n = 71, p = 0.1443). Co-feeding occurred only rarely (overall median = 1), between zero and 15 times per dyad across the entire observation period, and the species-specific medians varied only slightly between zero times (M. margotmarshae, M. myoxinus), 0.5x (M. danfossi, M. ravelobensis), 1x (M. bongolavensis) and 2x (M. mamiratra) across the 9-18 hours of observations per dyad. Given the rarity of this behavior, this behavior was not submitted to statistical modelling.

3.2.2 Variation in rates of agonism and number of conflicts among dyad types and species Individuals showed aggressive behaviors towards their dyad partners on average 2 ± 4.3 times per hour outside the sleeping box and varied between zero and 36.0 times across all individuals. Aggression rates could potentially be influenced by species (species model),

23 forest type (forest model), the phylogenetic background (clade model), the presence of a reproductively active female (repro model) in the dyad, but also by the individual dyad (random factor), the sex of an individual or the dyad type (mf or mm). In a first step, the relative suitability of the first four models to explain aggression rates was tested, whereas the sex and dyad type entered the models only afterwards. Three models, the species, forest, and clade model, provided a significantly better fit to the data than the null model (Table 3.8, Test 1, models #2 - #4) and performed equally well. In all three models, the addition of the dyad type and sex improved the fit significantly and a choice between them was not possible at that stage (Table 3.8, Test 2 models #6 - #8). However, within mf-dyads, the species model fitted the data best when sex was included as a further variable (Table 3.8, #10, Figure 3.4). A Tukey test revealed that M. mamiratra and M. margotmarshae had significantly higher aggression rates than all other species, whereas both species differed from each other only by a statistical trend (Estimate = 0.5798, SE = 0.2119, z = 2.737, p = 0.0682). Moreover, males had significantly lower aggression rates than females, which was particularly evident in M. margotmarshae and M. mamiratra (Figure 3.4).

Figure 3.4 Aggression rates in mf-dyads for each species and sex separately (interval frequency/hr both outside box). Mean, box: standard deviation, whiskers: minimum, maximum.

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In mm-dyads, only the forest model (Table 3.8, #15) performed significantly better than the null model with mm-dyads in humid forest showing significantly higher rates of aggression than those living in dry forests (Table 3.8, Figure 3.5).

Figure 3.5 Aggression rates in mm-dyads for each forest type (interval frequency/hr both outside box). Mean, box: standard deviation, whiskers: minimum, maximum

A total of 2101 conflicts were observed across the entire study period. The number of conflicts between pair partners varied widely between zero and 313 conflicts (mean = 29.6 ± 53.3 SD) per dyad and these were not significantly correlated with the joint space use of dyad partners (Spearman Rank correlation test, rS = -0.1003, n = 71, p = 0.405). All four models (species, forest, clade, repro) performed significantly better than the Null model, but the species model fitted the data best (Table 3.9, #2). The interaction of species*pair type improved the model significantly (#6) and both dyad types were therefore modelled separately (Table 3.9). The species model (#8) performed best among all four models (#8 - #11) for the mf- dyads (Table 3.9, Test 2) and revealed that mf-dyads of M. mamiratra had significantly more conflicts than those of any other species Table 3.9, Fig. 3.6). No other significant difference was detected. The number of conflicts in mm-dyads could not be explained by one model

25 alone, but the species model (#13), the forest model (#14) and the clade model (#15) all showed a significant fit to the data, indicating that mm-dyads in (1) M. mamiratra had significantly higher conflict numbers than M. myoxinus, (2) humid forests had higher conflict numbers than those in dry forests, and that (3) mm-dyads from the western and northwestern clade had significantly lower conflict numbers than those in the northern clade.

Figure 3.6 Species comparison of the total number of conflicts per dyad type. Mean, box: standard deviation, whiskers: minimum, maximum

3.2.3 Variation in social dominance among dyad types and species The total number of conflicts won by each dyad partner was used to determine whether social dominance could be statistically confirmed within each dyad (Table 3.9). Intersexual dominance was detected in 16 of 36 mf-dyads (44.4%) but these were not evenly distributed between species (Table 3.1). Species ranged from no female dominance (M. myoxinus) via rare female dominance (M. ravelobensis, M. bongolavensis), and moderate female dominance (half of the dyads showing female dominance, M. danfossi and M. margotmarshae) to unambiguous female dominance (M. mamiratra) where all female were dominant over their male partners. In contrast, only one case of male dominance could be detected (M. margotmarshae). Across all six dyads, females won significantly more conflicts

26 than males in two species only, M. danfossi and M. mamiratra (Table 3.1). Female dominance did not depend on body mass differences, as dominant females were partly lighter (n = 6), heavier (n = 7) or equal in body mass (n = 2) to their male dyad partners (Table 3.10). Table 3.1 Number of won conflicts for males and females in male-female dyads and their statistical comparison N Median Quartile Min-Max Wicoxon test Dominance Species m f m f m f z p m f M.myoxinus 6 0.5 1 0-1 0-1 0-2 0-3 0.404 0.686 0 0 M. ravelobensis 6 0.5 2 0-2 0-9 0-2 0-14 1.604 0.109 0 2 M. bongolavensis 6 0 2 0 0-4 0-4 0-8 1.095 0.273 0 1 M. danfossi 6 0.5 8 0-3 1-25 0-4 1-41 2.201 0.028 0 3 M. margotmarshae 6 1.5 13.5 0-9 2-25 0-16 1-142 1.572 0.116 1 3 M. mamiratra 6 4 101 3-5 48-196 1-10 46-298 2.201 0.028 0 6 Min-Max: minimum to maximum value, m: male, f: female, bold: p<0.05, dominance: number of mf dyads with male or female dominance

Male-male dominance was detected only in four out of six species and within these in 13 of 23 dyads (56.5%, Table 3.2). Species varied between 0% dyads with male dominance (M. myoxinus, M. ravelobensis) to 66.7% dyads with male dominance (M. bongolavensis, M. mamiratra). The number of significant dominance relationships in mf-dyads and mm-dyads per species did not correlate with each other (Spearman Rank correlation test, rs = 0.478, n=6, n.s).

Table 3.2 Number of male-male-dyads with significant male-male dominance per species Species N Dominance M.myoxinus 6 0 M. ravelobensis 6 0 M. bongolavensis 5 4 M. danfossi 6 2 M. margotmarshae 6 3 M. mamiratra 6 4 N: total number of dyads, Dominance: number of dyads with male dominance

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3.3 Discussion The aim of this study was to analyze and compare the patterns of social tolerance (i.e., patterns of affiliation) and its outcomes (i.e. aggression rates, no. of conflicts and social dominance) between six species of mouse lemurs that belong to different phylogenetic clades, inhabit different forest types and were studied in different reproductive periods. For a solid interpretation of the results, however, it is first essential to evaluate, if all putative affiliation parameters indeed reflect social tolerance between dyad partners. This is important, since the animals were most likely not familiar with each other and were kept together in temporary confinement in a cage setting. Under these circumstances, putative signals of social tolerance such as the joint stay in sleeping box or the joint stay in one cage compartment (joint space use) could also reflect a crypsis response [46] and point towards a lack of habituation [47]. This question was addressed by correlating the purely spatial parameters (joint stay in sleeping box, joint space use) with an intrinsically meaningful parameter, the interval frequency of non-agonistic body contacts. This analysis revealed that the joint stay in the sleeping box is most likely not reflecting true affiliation between the dyad partners, since there was no correlation detected with the total number of non-agonistic body contacts. The joint stay in the sleeping box was highest in M. myoxinus (Figure 3.1), although this species showed rather low frequencies of non-agonistic body contact (Figure 3.3). We therefore conclude that the joint stay in the sleeping box is reflecting some degree of disturbance that was experienced by the dyads during observations. Whereas the conditions for the behavioral observations themselves were always identical (e.g., distance between observer and cage, light regime, cage dimensions and furbishing), this was not the case for the external conditions. When working with M. myoxinus, the cages were placed under trees not far from the next village (for safety reasons), and there was a path leading close by that was frequented by villagers even at nighttime. It is likely that this external source of disturbance may have negatively influenced the behavior of the animals in the cages, i.e., they were hiding longer in the sleeping boxes than the other species. As a result, this parameter will not be included in the subsequent discussion of social tolerance. In contrast, there was a positive correlation between total body contacts and the joint space use (p < 0.0001), but no correlation between joint space use and the number of conflicts (n.s.). This parameter can thus be confirmed to be useful for the description of affiliation and thereby social tolerance between individuals.

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3.3.1 Influence of phylogeny on social tolerance Phylogenetic relatedness has previously been shown to influence and constrain a wide variety of behavioral patterns in primates ranging for example from feeding habits [48], patterns of reproduction [35], cognitive function [49, 50], communication [51-53], dominance styles [54, 55], to infant rearing systems [56, 57]. We therefore hypothesized that the social tolerance patterns of the six studied mouse lemur species may reflect their membership in three phylogenetic clades that were well supported in several previous phylogenetic studies [27, 58-60]. However, there was only relatively weak support for phylogenetic effects on social tolerance and its outcomes in mouse lemurs (Table 3.3). The models revealed significant support for the clade model only for three variables (joint space use, total body contact, number of conflicts) and only for male-male dyads. Furthermore, in all three cases, the support was not exclusive for the clade model, but significant support also existed for the forest model and/or the species model. Concerning the agonistic behavior (aggression rates, no. of conflicts, Figure 3.4, Figure 3.6), the four species of the northwestern and western clade (M. myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi) showed rather similar patterns, but typically differed from one or both members of the northern clade (M. mamiratra, M. margotmarshae). However, members of the same clade were not always similar in their behavior. For example, male-female dyads of M. bongolavensis showed significantly more joint space use and total body contacts than M. danfossi, and the number of conflicts was significantly higher in mf- dyads of M. mamiratra than of M. margotmarshae.

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Table 3.3 Summary of findings on parameters that explained variation in social tolerance and its outcomes

Pair Parameter Clade Forest Repro Species Directionality type

Being together in Mmyo > Mbon, Mmar Mmam // both - - - X sleeping box Mmam < Mdan, Mrav mf - - - X Mbon > Mdan Joint space use: Mmar > Mrav, Mbon, Mdan // variable pair mm X X - X HF > DF // type N>NW Total body mf - - - X Mbon > Mmyo, Mdan contact: HF > DF // variable pair mm X X - - N > NW type co-feeding - - - - Too few data Mmam Mmar > Mmyo, Mrav, Aggression rates mf - - - X Mbon, Mdan // M < F mm - X - - HF > DF Mmam > Mmar, Mdan, Mbon, mf - - - X No. of conflicts: Mrav, Mmyo variable pair Mmam > Mmyo // type mm X X - X HF > DF // N > NW, W

Intersexual Mmam > Mmar, Mdan > rest mf - - x x dominance (qualitatively) Mmam, Mbon > Mmar, Mdan > mm-dominance mm - - - x rest (qualitatively) Mmyo: M. myoxinus, Mrav: M. ravelobensis, Mbon: M. bongolavensis, Mdan: M. danfossi, Mmar: M. margotmarshae, Mmam: M. mamiratra, mm: male-male dyads, mf: male-female dyads X: statistical support from mixed models, x: qualitative support from tabulated data

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3.3.2 Influence of habitat type on social tolerance Based on temperature and rainfall data [35], the warm lowland evergreen rainforests inhabited by M. mamiratra and M. margotmarshae at the northern end of the study region are the least seasonal habitats and contrasted largely with the dry deciduous forests where the other four mouse lemur species occurred. It was hypothesized that species inhabiting the dry forests should be energetically more constrained by seasonal food scarcity during the dry season than those living in humid forests [61]. Whereas the dry forests in northwestern Madagascar do receive almost no rain during the dry season, the lowland rainforest further north receives precipitation during every month of the year, albeit some seasonal fluctuations in the amount [62]. As a consequence, species in dry forests should be more competitive when confronted with a monopolizable resource (one clumped feeding bowl) and show higher levels of agonism and lower levels of social tolerance than species inhabiting the humid forest, who may not need to compete for food resources due to the higher plant productivity in their environment [42]. The statistical tests revealed ambiguous support for this hypothesis (Table 3.3). Forest models were statistically supported only in male-male dyads in most parameters, but the effect was not always as expected. Whereas male-male dyads in humid forests showed indeed higher social tolerance (joint space use, total body contact) than those in the dry forest (in line with the expectation), they also had higher aggression rates and more agonistic conflicts than those in the dry forest (in contrast to the expectation). Male-female dyads in humid vs. dry forest did not differ significantly neither in social tolerance nor its consequences (Table 3.3). Whereas the mf-dyads of M. bongolavensis (dry forest) showed the highest average level of social tolerance (joint space use and total body contact) of all species, aggression rates and number of conflicts were highest in M. mamiratra followed by M. margotmarshae (both humid forest). Two main potential arguments could explain why the levels of social tolerance and its outcomes in mf-dyads did not follow expectations in this study. Aggression rates and the number of conflicts may be low in the dry forests because mouse lemur species may be primarily adapted to save energy during periods of food shortage and to avoid competition for resources [39]. Known energy-saving strategies from previously studied mouse lemur species include the accumulation of fat reserves in the tail (M. murinus - [63]), the use of daily or prolonged periods of torpor (reviewed in [64], M. murinus - [65], M. lehilahytsara – [66, 67]), reduced overall activity (M. murinus, [69]), and the formation of sleeping groups that have been shown to convey thermoregulatory benefits to their members

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(M. murinus, [68]). It is also possible that mouse lemurs actively avoid potentially competitive situations (e.g. close proximity at food resources) during the dry season, as social encounters at food resources are only rarely observed under natural conditions (M. murinus - [69], M. murinus and M. ravelobensis - [70]). The rarity of co-feeding bouts between dyad partners across all species in this study may further support this assumption. Such energy saving strategies may not be essential when living in a resource-rich environment such as a lowland evergreen rainforest and these species could therefore be less constrained in their social energy expenditure. Further studies are needed to clarify which of the abovementioned strategies may be employed by the four species studied in dry forests in this study. The lack of aggression and conflicts in the dry forest species may also be due to a lack of reproduction and therefore a reduced need for inter- and intrasexual conflicts. In fact, both rainforest species showed signals of reproduction with females of three dyads in each species being either pregnant (n = 1), recently in estrous (n = 3), shortly before estrous (n = 1), or lactating (n = 1, Table 3.4). However, there were even five females with signals of reproduction in M. danfossi (dry forest), including two females in estrous and one being pregnant (Table 3.4), and this species did not show significantly elevated aggression rates (Figure 3.4, Table 3.3) or a higher total number of conflicts (Figure 3.6, Table 3.3). This argument alone can therefore not explain the results of this study. It is possible, though, that the two mentioned possible explanations (energy-saving strategy, elevated conflict behavior during reproduction) are not exclusive but could be acting simultaneously and thereby could explain the mixed findings with regard to forest type.

3.3.3 Influence of reproductive activity on social tolerance It is known from the Gray Mouse Lemur (M. murinus) that males can compete severely for the access to estrous females under natural conditions (M. murinus, [15]) and in captivity (M. murinus, [71]), and that conflict rates among the sexes are higher and female dominance is more expressed in the reproductive season than in the non-reproductive season in captivity (M. murinus, M. lehilahytsara, [38]). It was therefore predicted that social tolerance (i.e. joint space use, total body contact) should be lower and agonistic rates should be higher when females are reproductively active in the population or in the dyad. It needs to be stated, though, that the period of reproductive activity of the six study species was not known prior to this study and was only established in parallel [35]. In retrospective, this prediction implies that three species, M. mamiratra, M. margotmarshae and M. danfossi, should have shown similarly low levels of social tolerance, higher aggression rates/number of

32 conflicts, and should have contained more dyads with clear dominance relationships and female dominance than the other species that did not contain reproductively active females (Table 3.4). However, the only detected similarity between the three species was that they contained the highest number of female dominant dyads (FDD) with either 50% FDD (M. margotmarshae, M. danfossi) or even 100% FDD (M. mamiratra) (Table 3.1) in contrast to the other three nonreproductive species that ranged between 0% FDD (M. myoxinus) to 33% FDD (M. ravelobensis). Besides, no single statistical model was in support of the predicted patterns (Table 3.3). Not only did these three reproducing species not all show lower social tolerance levels than the non-reproductive species, they also did not share high levels of aggression or conflict numbers (Figures 3.2-3.6). Instead, M. danfossi showed rather similar results in almost all analyses to the other mouse lemur species living in the dry forests, whereas M. mamiratra and M. margotmarshae showed intermediate tolerance levels and high aggression rates in both dyad types. It was argued in the previous chapter that M. danfossi may not have shown comparative patterns of agonism, because it may be under higher energetic constraints than the two northern species due to its life in highly seasonal dry forests. To investigate this hypothesis in more depth, further studies are needed to investigate with a comparative approach the energetic constraints, energy-saving strategies, and the basal metabolic rates of these six species. Alternatively, the two northern species (M. mamiratra, M. margotmarshae) may have higher aggression rates and more conflicts for another reason and not because of the presence of reproductive females in the population. Given that socioecological data are currently not available on their resource use (food, shelter), sleeping group composition, ranging behavior, and mating system, however, this possible explanation cannot be evaluated at present.

3.3.4 Interspecific variability in social tolerance and implications for social diversity in mouse lemurs The comparative evaluation of the clade model, forest model and repro model against a simple species model revealed that in male-female dyads, the variation in all parameters could be best explained by species-specific differences and not by phylogenetic clade membership, the forest type or the presence of reproductively active females in the population or dyad. This overall support for the simple species model is the consequence of single species acting as outliers in the analyses (Table 3.3). This was the case in the joint space use (M. bongolavensis high, M. danfossi low), total body contact (M. bongolavensis high),

33 aggression rates (M. mamiratra and M. margotmarthae high), number of conflicts (M. mamiratra high), female dominance (M. mamiratra high) male-male dominance (M. mamiratra and M. bongolavensis high). Given this distribution, two species, M. bongolavensis and M. mamiratra, require a separate discussion. Male-female dyads of M. bongolavensis were characterized by strikingly high social tolerance, i.e., dyad partners stayed on average more than half of the intervals (57.8%) together in the same cage compartment and also had the highest average values of total body contacts of all species. It is known that the reproductive period of M. bongolavensis starts towards the end of August (Radespiel, Rakotondravony unpubl. data) and none of the trapped females was showing signs of estrous in the current study that finished around Mid- August (9th July – 13th August). It is, however, possible that the males were already quite interested in the females and approached them frequently and maintained proximity during the observations. It is known from gray mouse lemurs that males start actively searching in an enlarged home range for estrous females even one month before the onset of the reproductive season [72], whereas females do not change their use of space, but announce their receptivity by vocal and olfactoric signalling [73]. Unfortunately, no data are available on the frequency of approaches by males versus females of M. bongolavensis in the cage experiments, so that it cannot be decided, which sex was responsible for the proximity between them. Since this elevated proximity was not accompanied by elevated aggression rates or conflict numbers (Figure 3.4, Figure 3.6, Table 3.1), though, it can be assumed that the females at least tolerated the males, which is unusual, at least in gray mouse lemurs [74, 75]. Interestingly, male-male dyads of M. bongolavensis had among the highest number of clear dominance relationships (n=4), and their conflict numbers were also slightly elevated (Figure 3.6). These findings suggest increased levels of intrasexual competition among males prior to the onset of mating activities, which has been described from the gray mouse lemur [71]. Interestingly, although M. myoxinus was also studied one month prior to the onset of estrus (study period: 9th September – 13th October; estrus may start in October, [35], it did not show the same behavioral pattern as M. bongolavensis. This suggests that social tolerance in mouse lemurs is multi-facetted and not easily explained by single parameters. Mf-dyads of M. mamiratra were different from the other species in various ways. They were very active (rare use of sleeping box), had intermediate levels of social tolerance, showed very high female aggression rates, high conflict numbers and unambiguous female dominance, i.e. all females won significantly more conflicts than their male partners. The difference between the number of conflicts won by males (median = 4, min = 0, max = 10)

34 and by females (median = 101, min = 46, max = 298) was strikingly larger than in any of the other species (Table 3.1). As females in this species had all very different reproductive states (3x no estrous, 1x pro-estrous, 1x recently in estrous, 1x pregnant), these consistently high values cannot be explained with a specific reproductive state (Table 3.4). In addition, four out of six male-male dyads had significant male-male dominance relationships, indicating elevated levels of male intrasexual competition even when not being in contact with females (Table 3.3, Figure 3.6). There are no socioecological data available on this species and therefore it is not known for example, whether or not they form sleeping groups, compete for some form of resources (e.g., food or shelter), have overlapping home ranges, or which kind of mating system they have. A recent study suggested that they, together with M. margotmarshae, may be exceptional within mouse lemurs as they may have a less seasonal reproduction than the other species studied so far [35]. A release from seasonality may increase the monopolization potential and therefore could result in higher contest competition in males [15]. However, the costs and benefits of sociality in males and females, the underlying competitive regimes and the proximate and ultimate reasons for their very strong female dominance cannot be inferred for this species from these first datasets. Finally, one interesting result of this study is the variable expression of female dominance among and within the six study species. Whereas no signals of female dominance were evident in M. myoxinus due to an overall scarcity of decided conflicts (n = 10) across all dyads, one female-dominant dyad (FDD) was detected M. bongolavensis (n = 1), two in M. ravelobensis (33% FDD), 50% FDD were apparent in M. danfossi and M. margotmarshae and all dyads were FDD in M. mamiratra (see above). Previous studies have already pointed towards some variability of this trait in mouse lemurs [23, 24] and suggested that this variability may be ultimately explained by variations in sex-specific energetic constraints that the species underwent in their ancestral habitats and by differences in the species-specific social organization. Given the relatively small geographic distribution of the mouse lemur species studied here, one can assume that the ancestral habitats were probably similar to the ones observed today, i.e., dry deciduous forests and lowland evergreen rainforests of northwestern to northern Madagascar. However, to evaluate the differences between the species in more depth, it would be important to compare dominance data that were all collected during the same reproductive period [24], i.e., either within or outside the period of reproduction. As it is, only the patterns between (1) M. myoxinus, M. ravelobensis and M. bongolavensis, as well as the pattern between (2) M. danfossi, M. margotmarshae and M. mamiratra can be directly compared. The difference between these two subgroups may be

35 attributed to difference in reproductive period. Whereas the species within the first group differed only gradually and no further interpretation can be made at this point, the uniqueness of M. mamiratra was already discussed above.

3.4 Conclusions This study revealed substantial evidence for variation in social tolerance (i.e., the patterns of affiliation) and its outcomes (i.e., aggression rates, number of conflicts and social dominance) within mouse lemurs, one of the most speciose radiations of lemurs in Madagascar. Whereas some variation can be explained by ecological factors, imposed either by variable energetic constraints in different forest environments (dry forest, rainforest) or by differences in reproductive activity, other species-specific differences cannot be easily understood. For example, social tolerance levels differed between M. bongolavensis and M. myoxinus, although both were studied within the same reproductive period and in the same forest type, and M. mamiratra and M. margotmarshae differed in agonism and female dominance, despite inhabiting the same forest type and containing reproductively active females. These findings suggest that the regulation of social tolerance is much more complex than previously thought and that species show strong signals of behavioral plasticity. Several authors have criticized over the last decade the increasing number of lemur species that have been scientifically described based mainly on genetic results (e.g., [76-78]). Results like the ones presented here show, however, that the different taxa also behave differently in a standardized social encounter paradigm. Under the concept of integrative taxonomy [79, 80], these findings can therefore be interpreted as further support for the taxonomic distinctiveness of these taxa and their correct classification as species.

3.5 Methods 3.5.1 Study sites and study species This study was conducted at six sites (Bombetoka, Ampijoroa, Marosely, Anjiamangirana, Ankaramibe and Lokobe) situated in six Inter-River-Systems (IRS 0, I, II, III, V and IRS VI) [81] from western to northern Madagascar (Figure 3.7, Table 3.4). All six species are threatened by habitat loss in their natural habitats and are therefore classified as endangered (EN, Microcebus myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi, M. margotmarshae) or critically endangered (CR, M. mamiratra) according to the IUCN red list [82]. The study species differ in forest type (dry deciduous forest vs. evergreen humid forest), their clade membership (clades 1, 2, 3), and the presence or absence of reproductively active

36 females in the population (Table 3.4). For logistic reasons (not all field sites are accessible throughout the whole year) all field work took place during the two successive dry seasons from May to October 2015 and 2016.

Figure 3.7 Map with northern half of Madagascar showing study sites of six study species. 0- VI: Inter-River-Systems. Geographic coordinates area provided in Table 3.9.1

3.5.2 Capture and selection of study animals At all dry forest sites, Microcebus spp. were captured with Sherman live traps (HB Sherman Traps Inc., Tallahassee, FL), baited with banana slices according to established methods [35, 81, 83], whereas they were captured by hand in the two humid forest sites. Captured animals were sexed, weighed and marked according to established protocols [81, 83]. Dyad partners for social encounter experiments were selected based on comparable body mass and on being trapped as far away as possible from each other (mf-dyads: median = 244m, quartiles = 128 – 1145m, minimum = 25m, maximum = 2406m, N=36; mm-dyads: median = 350m, quartiles = 88 – 1140m, minimum = 0m, maximum = 2549m, N=35). For individual identification during the nocturnal observations, one animal of each dyad was marked with a fur cut on the tail. Animals not selected for social encounter experiments were released at their trapping site in the early evening. As a rule, a total of six male-male and six male-female dyads were formed and observed for a maximum of six nights in each species following the night of capture. As an exception and due to capture problems, we formed only 37 five male-male dyads in M. bongolavensis. All animals were released after one week at their individual capture point after the end of the last night of observations.

3.5.3 Experimental set-up and data collection The social encounter experiments were conducted in cages of about 1m3 that were equipped with four wooden bars and two sleeping sites (Figure 3.8, [84]). Cages were placed in the forest close to the research camp but >1 km away from the capture sites. Animals were fed daily with banana and received water ad libitum. Furthermore, they had access to arthropod prey that entered their cages naturally during the night. Only one shelter was available for the dyad partners during observations, while both were accessable outside those times. This approach was chosen to promote social interactions between the partners. Each cage was divided in 8 compartments of equal size [upper front (A, D) upper back (B, C), lower front (E, G), lower back (F, H)] in addition to the roof, floor, shelter, and feeding station.

Figure 3.8 Encounter cage with eight compartments (A-H) and four extra locations (Ro, T, S, FS). One sleeping box (S) was attached per side. Food was presented on the cage floor in a bowl (FS). Upper and lower front and back compartments were equipped with one wooden bar each

3.5.4 Behavioral observations Observations were perfomed on each dyad during three hours per night over six consecutive nights between 06h00 p.m. and 09h00 p.m. in 67 of the 71 dyads (94.4%) of the dyads. Two mm-dyads of M. myoxinus and one mf-dyad of M. ravelobensis were only observed during five nights, and one mm-dyad of M. myoxinus was only observed during three nights. Observations ended earlier than planned in these cases due to an unintentional

38 escape of the animals from their cages. During observations, a team of two observers sat motionless in two meters distance to the cage and started a protocol when the animals woke up. The observers utilized a headlamp and Maglite torch with red filter to obtain better visibility. Protocols were recorded on a digital Dictaphone (Sony). The use of the 12 locations in the cage was noted every 15 sec for both pair partners by means of instantaneous sampling [85]. All occurrences of feeding at the feeding station and of social behaviors of both partners were noted whenever they occurred. Social behaviors consisted (1) of affiliative behaviors (unspecific body contact, allogrooming) that were added up for the purpose of this study to “total body contact”, and (b) of agonistic behaviors (aggressive (A): fighting, chasing, biting, displacing; submissive (S): fleeing, avoidance, for definitions see [86]). A conflict was defined as a series of agonistic behaviors that was not interrupted for more than one second [86]. A conflict was defined as decided, if (a) one animal behaved aggressively (e.g., chase, displace) and the other one reacted submissively (e.g., fleeing)(AS), (b) one animal avoided the other (OS), or (c) if a physical fight ended in a flight of one opponent (AAS). Decided conflicts were used to infer social dominance among the dyad partners of the same or opposite sex. Social dominance was determined in each dyad separately by means of a Binomial test (http://www.socscistatistics.com/tests/binomial/Default2.aspx), and the overall evidence for intersexual dominance was analysed for each species by means of a Wilcoxon Matched Pairs Test conducted in Statistica 6.0 (StatSoft Inc., Tulsa, OK). We inferred social tolerance between the dyad partners by the following behavioral parameters: (a) Joint stay in sleeping box: Number of 15s-intervals being together in the sleeping box per hour of observations. (b) Joint space use: Number of 15s-intervals of staying together in one of the eight compartments or on roof or floor of the cage per hour that both animals spent together outside the sleeping box. (c) Total body contact: Number of 15s-intervals in non-agonistic body contact outside the sleeping box per hour that both animals spent together outside the sleeping box. We inferred the outcomes of social tolerance between the dyad partners by the following behavioral parameters: (d) Co-feeding: number of times that both partners were eating together at the feeding bowl.

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(e) Aggression rate: Number of individual aggressive behaviors per hour that both animals spent together outside the sleeping box. (f) Number of conflicts (see above for definition of conflict) (g) Social dominance (see above for definition of dominance)

3.5.5 Statistical modelling All spoken protocols were transferred to and edited in EXCEL 2010. Dependent variables were first tested regarding their departure from normal distribution and homogeneity of variances. If needed, data were transformed, either logarithmically (total body contact, aggression rate) or by square root transformation (joint space use, no. of conflicts). Determinants of variation in the joint stay in sleeping box, joint space use, total body contacts and the number of conflicts were inferred by means of comparative generalized linear models that were fitted with the gls-function and the use of maximum likelihood for the estimation of fixed parameters in RStudio 1.0.143 [87] with the package nlme. Each modelling procedure started with a null model (= no fixed factors) and a basic model that included only species as fixed factor. Model improvements were tested by means of the anova() function and the implemented Likelihood Ratio Test. Next, three alternative models were built with Clade (clade 1, 2, 3), Forest type (dry vs. humid) and reproduction of females in population (yes vs. no) as fixed factors, respectively. The relative improvement provided by these three models over the null model and the species model was compared by means of the anova() function and the best model was identified by the smallest AIC value given the results of the Likelihood Ratio test. Next, we added the dyad type (mm vs. mf) as second fixed factor to the best model to test for an improvement of the model fit. If the model was improved significantly, separate models were then fitted to two subsets of the data representing the two dyad types, respectively. Whenever more than two elements were included in one significant factor such as in species (six elements = species) and clade (three elements = clades), a posthoc test was conducted (Tukey) to identify which species or clades differed significantly from each other. In order to infer the determinants of the aggression rate of individuals, a mixed-effect model was built with the lme-function and the use of maximum likelihood for the estimation of fixed parameters in RStudio 1.0.143. Pair identity was introduced as random factor, since the behavior of both partners could influence each other. Modelling steps followed those described above with two modifications. First, we used the reproductive status of the paired female as potential determinant of aggression rate of both pair partners (repro) instead of the

40 presence of reproductively active female in the capture population. Second, when dyad type contributed significantly to model improvement, sex (male, female) was introduced as an additional fixed factor to test whether the sexes differed systematically in their aggression rates in mf-dyads.

3.6 Declarations 3.6.1 Ethics approval As these species are not kept in breeding colonies worldwide but fundamental research on them is urgently needed, it was necessary to study wild animals in Madagascar. The objective of the proposal research is consistent with priorities for Malagasy primate conservation: conducting ecological and behavioral studies to determine the identity and requirements of endangered populations and species. In agreement with German law, the University of Veterinary Research Hannover, Germany, does not yet have an ethics committee to review field studies conducted in other countries. The research nevertheless fully complied with the legal requirements of Madagascar, the country in which the research was conducted (Permission no. 074/15/MEEMEF/SG/DGF/DCB.SAP/SCB, 130/16/MEEF/SG/DGF/DAPT/SCBT.Re), and adhered to the ARRIVE guidelines, the ethical guidelines of the International Council of Laboratory Animal Science (ICLAS), the IUCN Policy Statement on Research Involving Species at Risk of Extinction, and the Principles for the Ethical Treatment of Non-Human Primates of the American Society of Primatologists (https://www.asp.org/society/resolutions/EthicalTreatmentOfNonHumanPrimates.cfm).

3.6.2 Consent for publication Not applicable

3.6.3 Availability of data and material The dataset generated and analysed during the current study is available from the corresponding author on reasonable request.

3.6.4 Competing interests The authors declare that they have no competing interests.

3.6.5 Funding This study was funded by a scholarship from DAAD (Deutscher Akademischer

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Austauschdienst, German Academic Exchange Service), granted to MRE and AFH, by a grant to cover some costs of the field work of the Rufford Small Grants Foundation granted to AFH, and by the Institute of Zoology, University of Veterinary Medicine Hannover, Germany.

3.6.6 Author’s contributions EZ initiated this study and guided the zoological part in Madagascar. EZ and UR conceived and designed the study. MRE and AFH collected the data. MRE and UR analysed the data and drafted the manuscript. UR instructed the statistical analyses of the data. All authors participated in the interpretation of the data. All authors read and approved the final manuscript.

3.7 Acknowledgements The authors thank the DGF (Ministère De L’Environnement, de L’Ecologie et des Forêts de Madagascar), MNP (Madagascar National Parks), MAAF (Madagascar Aye-aye Foundation), Lokobe National Park, Ankarafantsika National Park and their Staff, as well as Mahajanga University for permission to work on this project and for their help to conduct the necessary field work. Furthermore, the authors are endebted to the students Hasinirina A.S. Andriamendrikaja, Ursulla L.Z. Mahatoly, Sandra P. Ratsimbazafy, Etangie Radelin from the Faculty of Science at Mahajanga University for their assistance in the field. The authors are grateful to the people who helped capturing the animals and guiding them in the forest: Jean Dé Rakotoarimanana, Jean Arsène, and Dadabe (Ankarafantsika National Park); Xavier (Marosely); Janardana Hasina Razanadahy, Lahantsoa, and Ben Said (Bombetoka); Anjara Jean Joel, Anuar Aly, and Amady Saidaly (Nosy Be); David, Etienne, Patrice, and Tsaraleha (Ankaramibe); Taoro, Justira, Beanjara, and Mainty (Anjiamangirana). Moreover, the authors are grateful to everybody who helped to set up and maintain the field camps. Finally, the authors are grateful to Soenke von den Berg for technical support.

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(Microcebus murinus) and the golden-brown mouse lemur (M. ravelobensis), in northwestern Madagascar. Int J Primatol. 2011; 32(3):566-86. 71. Perret M. Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus) Folia Primatol. 1992; 59:1-25. 72. Schmelting B. Reproductive tactics in male grey mouse lemurs (Microcebus murinus, J.F. Miller 1777) in Northwestern Madagascar [Thesis]. Hannover: Tierärztliche Hochschule; 2001. 73. Buesching CD, Heistermann M, Hodges JK, Zimmermann E. Multimodal Oestrus Advertisement in a Small Nocturnal Prosimian, Microcebus murinus. Folia Primatol. 1998; 69 (Suppl.1):295-308. 74. Eberle M, Kappeler PM. Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus). Behav Ecol Sociobiol. 2004; 57(1):91-100. 75. Radespiel U, Zimmermann E. The influence of familiarity, age, experience and female mate choice on pregnancies in captive grey mouse lemurs. Behaviour. 2003; 140:301-18. 76. Markolf M, Brameier M, Kappeler PM. On species delimitation: Yet another lemur species or just genetic variation? BMC Evol Biol. 2011; 11:216. 77. Tattersall I. Madagascar's lemurs: cryptic diversity or taxonomic inflation? Evol Anthropol. 2007; 16(1): 12-23. 78. Zinner D, Roos C. So what is a species anyway? A primatological perspective. Evol Anthropol. 2014; 23(1): 21-3. 79. Padial JM, Miralles A, De la Riva I, Vences M. The integrative future of taxonomy. Front Zool. 2010;7(1):16. 80. Zimmermann E, Radespiel U. Species concepts, diversity, and evolution in primates: lessons tobe learned from mouse lemurs. Evol Anthropol. 2014;23(1):11-4. 81. Olivieri G, Zimmermann E, Randrianambinina B, Rasoloharijaona S, Rakotondravony D, Guschanski K, et al. The ever-increasing diversity in mouse lemurs: three new species in north and northwestern Madagascar. Mol Phylogenet Evol. 2007; 43(1):309-27. 82. Schwitzer C, Mittermeier R, Johnson S, Donati G, Irwin M, Peacock H, et al. Averting lemur extinctions amid Madagascar's political crisis. Science. 2014; 343(6173):842-3. 83. Zimmermann E, Cepok S, Rakotoarison N, Zietemann V, Radespiel U. Sympatric Mouse Lemurs in Nort-West Madagascar: A New Rufous Mouse Lemur Species (Microcebus ravelobensis). Folia Primatol. 1998; 69(2):106-14. 84. Hasiniaina AF, Scheumann M, Rina Evasoa M, Braud D, Rasoloharijaona S, Randrianambinina B, et al. High frequency/ultrasonic communication in a critically endangered nocturnal primate, Claire's mouse lemur (Microcebus mamiratra). Am J Primatol. 2018:e22866. 85. Altmann J. Observational study of behavior: sampling methods. Behaviour. 1974; 49:227-67. 86. Hohenbrink S, Koberstein-Schwarz M, Zimmermann E, Radespiel U. Shades of Gray Mouse Lemurs: Ontogeny of Female Dominance and Dominance-Related Behaviors in a Nocturnal Primate. Am J Primatol. 2015; 77(11):1158-69. 87. RStudio Team. RStudio: Integrated Development for R. Boston: RStudio, Inc.; 2015.

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3.9 Additional files Table 3.4 Descriptive data of study species Species, study site, forest type, latitude (South) and longitude (East) in decimal degree, clade, total number of individual males (M) and females (F) captured at each site, number of studied male-male (MM) and male-female (MF) dyads, study period and number of reproductively active females in observed dyads and in capture population. Study Females in Species Site FT South East Clade No. of ind. Study period RA% dyads dyads M. myoxinus Bombetoka DDF -15.883° 46.233° 3 18M, 15F 6MM, 6MF 09.09. - 13.10.2015 6CL 0 M. ravelobensis Ampijoroa DDF -16.317° 46.817° 2 15M, 25F 6MM, 6MF 30.04. - 14.06.2015 6CL 0 M. bongolavensis Marosely DDF -15.650° 47.583° 2 16M, 19F 5MM, 6MF 09.07. - 13.08.2015 6CL 0 1CL, 2O, M. danfossi Anjiamangirana DDF -15.150° 47.730° 2 22M, 23F 6MM, 6MF 17.09. - 22.10.2016 71.4 2RC, 1P M. margotmarshae Ankaramibe EHF -13.964° 48.198° 1 18M, 21F 6MM, 6MF 09.08. - 13.09.2016 3CL, 2RC, 1L 42.1 3CL, 1S, M. mamiratra Lokobe EHF -13.383° 48.333° 1 22M, 16F 6MM, 6MF 25.06. - 31.07.2016 46.2 1RC, 1P FT= forest type; DDF= dry deciduous forest; EHF= evergreen humid forest; No. of ind= number of individuals captured at each site; CL: closed; S: swollen; O: estrus; RC: recent closely; P: pregnancy; L: lactation; RA% = percentage of reproductively active females among all captured females

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Table 3.5 Statistical model for staying together in the sleeping box Statistical model comparisons and best model to explain the frequency of staying together in the sleeping box (SB) by the parameters species, phylogeny (clade), forest type (forest) or the presence of reproductive females (repro). First, all models were compared to Base 0 model (Test 1, LRT1, P1-values). Second, the three alternative models were compared to the species model (Test 2, LRT2, P2-value). Finally, pair type was added to the best model (#2) as an interaction term, but did not improve model fit. Model details for the best model are provided below. The best model is highlighted in bold and effect directions are included.

Model comparisons df AIC BIC logLiK Test 1 LRT1 P1-value Test 2 LRT2 P2-value Effect #1 Base 0 2 751.0158 755.5412 -373.5079 #2 Species 7 724.6198 740.4585 -355.3099 1 vs. 2 36.396 <0.0001 Mmyo > Mbon*, Mmar*, Mmam** */ Mmam < Mdan* *, Mrav*** #3 Forest 3 736.1427 742.9307 -365.0714 1 vs. 3 16.873 <0.0001 2 vs. 3 19.523 6e-04 #4 Clade 4 732.6426 741.6933 -362.3213 1 vs. 4 22.373 <0.0001 2 vs. 4 14.023 0.0029 #5 Repro 3 743.2985 750.0865 -368.6492 1 vs. 5 9.717 0.0018 2 vs. 5 26.679 <0.0001

#6 Species * pair type 13 730.8097 760.2245 -352.4048 2 vs. 6 5.810 0.4448

Best model: #2 Coefficient SE t-value p-value (Intercept) 154.70550 10.88210 14.216517 <0.0001

M. ravelobensis -15.40638 15.38961 -1.001090 0.3205 M. bongolavensis -53.60451 15.73549 -3.406600 0.0011 M. danfossi -28.34859 15.38961 -1.842061 0.0700

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M. margotmarshae -47.07258 15.38961 -3.058725 0.0032 M. mamiratra -90.98844 15.38961 -5.912330 <0.0001 Mmyo: M. myoxinus, Mbon: M. bongolavensis, Mrav: M. ravelobensis, Mdan: M. danfossi, Mmar: M. margotmarshae, Mmam: M. mamiratra. *: p <0.05, **: p<0.01, ***: p<0.001

Table 3.6 Statistical models for joint space use Statistical model comparisons and details of best models to explain the frequency of joint space use by the parameters species, phylogeny (clade), forest type (forest) or the presence of reproductive females (repro). First, all models were compared to Base 0 model (Test 1, LRT1, P1-values), Second, the three alternative models were compared to the species model (Test 2, LRT2, P2-value). Pair type was added to the best model (#2) as an interaction term and improved the model significantly. Separate models were calculated and compared for mf-dyads and mm-dyads. Model details of the best models are provided. The best model and significant effects are highlighted in bold and effect directions are included.

Model comparisons - all df AIC BIC logLiK Test 1 LRT1 P1-value Test 2 LRT2 P2-value Effect #1 Base 0 - all 2 324.4300 328.9554 -160.2150 #2 Species- all 7 313.8421 329.6809 -149.9211 1 vs. 2 20.588 0.0010 #3 Forest- all 3 322.7763 329.5643 -158.3881 1 vs. 3 3.654 0.0559 2 vs. 3 16.934 0.002 #4 Clade- all 4 322.7267 331.7774 -157.3633 1 vs. 4 5.703 0.0577 2 vs. 4 14.885 0.0019 #5 Repro- all 3 326.1730 326.1730 -160.0865 1 vs. 5 0.257 0.6122 2 vs. 5 20.331 4e-04

#6 Species * pair type 1 309.3107 338.7256 -141.6554 2 vs. 6 16.531 0.0112 3

Model comparisons - mf

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#7 Base 0 – mf 2 171.3360 174.5030 -83.66798 #8 Species – mf 7 164.4063 175.4909 -75.20314 7 vs. 8 16.930 0.0046 Mbon > Mdan** #9 Forest – mf 3 173.2423 177.9929 -83.62116 7 vs. 9 0.0936 0.7596 8 vs. 9 16.836 0.0021 #10 Clade – mf 4 174.6842 181.0183 -83.34211 7 vs. 10 0.6517 0.7219 8 vs. 10 16.278 0.001 #11 Repro – mf 3 169.5889 174.3394 -81.79443 7 vs. 11 3.7471 0.0529 8 vs. 11 13.183 0.0104

Best model – mf: Coefficie SE t-value p-value nt #8 Species – mf (Intercept) 9.359034 0.8739943 10.708347 <0.0001 M. ravelobensis -1.787225 1.2360145 -1.445958 0.1586 M. bongolavensis 1.902952 1.2360145 1.539587 0.1341 M. danfossi -2.714330 1.2360145 -2.196034 0.0360 M. margotmarshae -0.152352 1.2360145 -0.123261 0.9027 M. mamiratra -1.681569 1.2360145 -1.360476 0.1838

Model comparisons - mm #12 Base 0 – mm 2 156.2953 159.4060 -76.14766 #13 Species – mm 7 145.3070 156.1944 -65.65349 12 vs. 13 20.988 8e-04 Mmar > Mrav*, Mbon*, Mdan** #14 Forest – mm 3 145.6342 150.3003 -69.81712 12 vs. 14 12.661 4e-04 13 vs. 14 8.327 0.0803 humid > dry*** #15 Clade – mm 4 145.1671 151.3885 -68.58355 12 vs. 15 15.128 5e-04 13 vs. 15 5.860 0.1186 N > NW*** #16 Repro – mm 3 156.1738 160.8399 -75.08691 12 vs. 16 2.1215 0.1452 13 vs. 16 18.867 8e-04

Best models – mm: Coefficie SE t-value p-value

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nt #13 Species – mm (Intercept) 8.813920 0.7082358 12.444894 0.0000 M. ravelobensis -0.861619 1.0015967 -0.860245 0.3967 M. bongolavensis -1.166582 1.0504835 -1.110519 0.2759 M. danfossi -1.859689 1.0015967 -1.856724 0.0735 M. margotmarshae 2.542484 1.0015967 2.538430 0.0168 M. mamiratra 0.477995 1.0015967 0.477233 0.6368

#14 Forest - mm (Intercept) 7.850409 0.3819405 20.554011 0e+00 Forest-humid 2.473750 0.6522876 3.792423 6e-04

#15 Clade - mm (Intercept) 10.32415 0.5183753 19.916381 <0.0001 9 Clade-nw -2.813813 0.6770470 -4.156009 0.0002 Clade-w -1.510239 0.8978523 -1.682058 0.1023 Mmyo: M. myoxinus, Mbon: M. bongolavensis, Mrav: M. ravelobensis, Mdan: M. danfossi, Mmar: M. margotmarshae, Mmam: M. mamiratra. *: p <0.05, **: p<0.01, ***: p<0.001

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Table 3.7 Statistical models for total body contact Statistical model comparisons and details of best models to explain the frequency of total body contact by the parameters species, phylogeny (clade), forest type (forest) or the presence of reproductive females (repro). First, all models were compared to Base 0 model (Test 1, LRT1, P1-values), Pair type was added to the species model (#2) as an interaction term and improved the model significantly. Separate models were calculated and compared for mf-dyads and mm-dyads. Model details of the best models are provided. Best models and significant effects are highlighted in bold and effect directions are included.

Model comparisons - all df AIC BIC logLiK Test 1 LRT1 P1-value Test 2 LRT2 P2-value Effect #1 Base 0 - all 2 250.1359 254.6613 -123.0680 #2 Species- all 7 249.1435 264.9823 -117.5718 1 vs. 2 10.992 0.0515 #3 Forest- all 3 250.7117 257.4998 -122.3559 1 vs. 3 1.424 0.2327 #4 Clade- all 4 252.3664 261.4171 -122.1832 1 vs. 4 1.770 0.4128 #5 Repro- all 3 252.0998 258.8879 -123.0499 1 vs. 5 0.036 0.8493

#6 Species * pair type 13 247.2564 276.6712 -110.6282 1 vs. 6 24.880 0.0095

Model comparisons - mf #7 Base 0 – mf 2 134.4115 137.5785 -65.2058 #8 Species – mf 7 132.6715 143.7561 -59.3358 7 vs. 8 11.740 0.0385 Mbon > Mmyo+, Mdan+ #9 Forest – mf 3 136.1564 140.9070 -65.0782 7 vs. 9 0.255 0.6135 8 vs. 9 11.485 0.0216 #10 Clade – mf 4 135.6658 141.9999 -63.8329 7 vs. 10 2.746 0.2534 8 vs. 10 8.994 0.0294 #11 Repro – mf 3 134.9527 139.7032 -64.4763 7 vs. 11 1.459 0.2271 8 vs. 11 10.281 0.036

Best model – mf: Coefficient SE t-value p-value

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#8 Species – mf (Intercept) 0.7170901 0.5624562 1.2749262 0.2121 M. ravelobensis 0.6683908 0.7954332 0.8402854 0.4074 M. bongolavensis 2.3800346 0.7954332 2.9921240 0.0055 M. danfossi 0.1878942 0.7954332 0.2362162 0.8149 M. margotmarshae 0.6836015 0.7954332 0.8594079 0.3969 M. mamiratra 0.4068131 0.7954332 0.5114359 0.6128

Model comparisons - mm Df AIC BIC logLiK Test 1 LRT1 P1-value Test 2 LRT2 P2-value Effect #12 Base 0 – mm 2 115.5961 118.7068 -55.79804 #13 Species – mm 7 115.1273 126.0147 -50.56363 12 vs. 13 10.469 0.063 #14 Forest – mm 3 110.4507 115.1167 -52.22535 12 vs. 14 7.145 0.0075 Humid > dry** #15 Clade – mm 4 111.2424 117.4638 -51.62122 12 vs. 15 8.354 0.0153 14 vs. 15 1.208 0.2717 N > NW ** #16 Repro – mm 3 116.2248 120.8908 -55.11239 12 vs. 16 1.371 0.2416

Best models – mm: Coefficient SE t-value p-value #14 Forest - mm (Intercept) 1.575111 0.2310520 6.817130 0.00 Forest-humid 1.078776 0.3945964 2.733872 0.01

#15 Clade - mm (Intercept) 2.653888 0.3192777 8.312159 0.0000 Clade-nw -1.224030 0.4170068 -2.935275 0.0061 Clade-w -0.667224 0.5530053 -1.206542 0.2365

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Mmyo: M. myoxinus, Mbon: M. bongolavensis, Mrav: M. ravelobensis, Mdan: M. danfossi, Mmar: M. margotmarshae, Mmam: M. mamiratra. +: p <0.1, *: p<0.05, **: p<0.01, ***: p<0.001

Table 3.8 Statistical model for aggression rate Statistical model comparisons and details of best models to explain aggression rate by the parameters species, phylogeny (clade), forest type (forest) or the presence of reproductively active females (repro). First, all models were compared to Base 0 model (Test 1, LRT1, P1- values), Pair type and sex were added to the models #2 - #4 and improved them significantly. Separate models were calculated and compared for mf-dyads and mm-dyads. Model details of the best models are provided. Best models and significant effects are highlighted in bold and effect directions are included.

Model comparisons - all df AIC BIC logLiK Test 1 LRT1 P1-value Test 2 LRT2 P2-value Effect #1 Base 0 - all 3 300.0916 308.9590 -147.0458 #2 Species- all 8 276.2015 299.8481 -130.1007 1 vs. 2 33.890 <.0001 #3 Forest- all 4 273.0640 284.8873 -132.5320 1 vs. 3 29.028 <.0001 #4 Clade- all 5 274.3016 289.0807 -132.1508 1 vs. 4 29.790 <.0001 #5 Repro- all 4 298.9368 310.7602 -145.468 1 vs. 5 3.155 0.0757

#6 Species + Type + Sex 10 256.1406 285.6988 -118.0703 2 vs. 6 24.061 <.0001 #7 Forest + Type + Sex 6 253.3205 271.0555 -120.6603 3 vs. 7 23.744 <.0001 #8 Clade + Type + Sex 7 254.5512 275.2420 -120.2756 4 vs. 8 23.750 <.0001

Model comparisons - mf #9 Base 0 - mf 3 173.7870 180.6170 -83.89351 #10 Species + Sex 9 127.8671 148.3571 -54.93356 9 vs. 10 57.920 <.0001 Mmam, Mmar >

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Mmyo***, Mrav*** ,*, Mbon***, Mdan ***,* #11 Forest + Sex 5 129.9441 141.3274 -59.97203 9 vs. 11 47.843 <.0001 10 vs.11 10.077 0.0392 #12 Clade + Sex 6 131.6623 145.3223 -59.83113 9 vs. 12 48.125 <.0001 10 vs. 12 9.795 0.0204

Best model – mf: Coefficient SE t-value p-value #10 Species + Sex (Intercept) 0.6630278 0.1702971 3.893361 0.0004 M. ravelobensis 0.2335494 0.2229712 1.047442 0.3033 M. bongolavensis -0.1263996 0.2229712 -0.566888 0.5750 M. danfossi 0.2062540 0.2229712 0.925025 0.3623 M. margotmarshae 0.8758513 0.2229712 3.928092 0.0005 M. mamiratra 1.4556179 0.2229712 6.528278 0.0000 Sex-m -0.5287337 0.1287325 -4.107228 0.0002 M < F

Model comparisons - mm Df AIC BIC logLiK Test 1 LRT1 P1-value Test 2 LRT2 P2-value Effect #13 Base 0 – mm 120.7162 127.4617 -57.35808 #14 Species – mm 123.9536 141.9416 -53.97679 13 vs. 14 6.763 0.2389 #15 Forest – mm 117.7190 126.7130 -54.85949 13 vs. 15 4.997 0.0254 Humid > dry* #16 Clade – mm 119.0803 130.3228 -54.54014 13 vs. 16 5.636 0.0597

Best model – mm: Coefficient SE t-value p-value #15 Forest - mm (Intercept) 0.4786832 0.1040305 4.601374 0.0001

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Forest-humid 0.4058431 0.1776659 2.284305 0.0289

Mmyo: M. myoxinus, Mbon: M. bongolavensis, Mrav: M. ravelobensis, Mdan: M. danfossi, Mmar: M. margotmarshae, Mmam: M. mamiratra. *: p <0.05, **: p<0.01, ***: p<0.001, if two significance levels are provided, the first refers to the first compared species and the second refers to the sec ond compared species.

Table 3.9 Statistical models for number of conflicts Statistical model comparisons and details of best models to explain the number of conflicts by the variables species, phylogeny (clade), forest type (forest) or the presence of reproductive females (repro). First, all models were compared to Base 0 model (Test 1, LRT1, P1-values). Second, the three alternative models were compared to the species model (Test 2, LRT2, P2-value). Pair type was added to the best model (#2) as an interaction term and improved the model significantly. Separate models were calculated and compared for mf-dyads and mm-dyads. Model details of the best models are provided. The best model and the significant effects are highlighted in bold and effect directions are included.

Model comparisons - all df AIC BIC logLiK Test 1 LRT1 P1-value Test 2 LRT2 P2-value Effect #1 Base 0 - all 2 387.0267 391.5521 -191.5134 #2 Species- all 7 352.3494 368.1882 -169.1747 1 vs. 2 44.677 <.0001 #3 Forest- all 3 356.7572 363.5453 -175.3786 1 vs. 3 32.270 <.0001 2 vs. 3 12.408 0.01 #4 Clade- all 4 357.6949 366.7456 -174.8475 1 vs. 4 33.332 <.0001 2 vs. 4 11.346 0.01 #5 Repro- all 3 371.5645 378.3526 -182.7823 1 vs. 5 17.462 <.0001 2 vs. 5 27.215 <.0001

#6 Species * pair type 13 340.4027 369.8176 -157.2014 2 vs. 6 23.947 0.0005

Model comparisons - mf

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#7 Base 0 – mf 2 210.5107 213.6777 -103.25533 #8 Species – mf 7 176.5906 187.6753 -81.29531 7 vs. 8 43.920 <.0001 Mmam > Mmar**, Mdan***, Mbon** *, Mrav***, Mmyo *** #9 Forest – mf 3 185.7988 190.5493 -89.89939 7 vs. 9 26.712 <0.0001 8 vs. 9 17.208 0.0018 #10 Clade – mf 4 187.4672 193.8013 -89.73361 7 vs. 10 27.043 <0.0001 8 vs. 10 16.877 0.0007 #11 Repro – mf 3 197.6857 202.4362 -95.84283 7 vs. 11 14.825 <0.0001 8 vs. 11 29.095 <.0001

Best model – mf: Coefficient SE t-value p-value #8 Species – mf (Intercept) 1.997383 1.035149 1.929560 0.0632 M. ravelobensis 0.784963 1.463922 0.536205 0.5958 M. bongolavensis 0.121746 1.463922 0.083165 0.9343 M. danfossi 1.481534 1.463922 1.012031 0.3196 M. margotmarshae 4.112628 1.463922 2.809322 0.0087 M. mamiratra 10.162545 1.463922 6.941998 <.0001

Model comparisons - mm #12 Base 0 – mm 2 168.8604 171.9711 -82.43021 #13 Species – mm 7 165.4998 176.3872 -75.74988 12 vs. 1 13.361 0.0202 Mmam > Mmyo* 3 #14 Forest – mm 3 161.2086 165.8746 -77.60427 12 vs. 1 9.652 0.0019 13 vs. 1 3.709 0.4469 Humid > Dry** 4 4 #15 Clade – mm 4 161.9587 168.1801 -76.97935 12 vs. 1 10.902 0.0043 14 vs. 1 1.250 0.2636 N > NW*, W**

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5 5 #16 Repro – mm 3 166.4658 171.1319 -80.23292 12 vs. 1 4.395 0.0361 15 vs. 1 6.507 0.0107 6 6

Best models – mm: Coefficient SE t-value p-value #13 Species – mm (Intercept) 1.609476 0.9450572 1.7030458 0.0993 M. ravelobensis 0.763493 1.3365128 0.5712574 0.5722 M. bongolavensis 2.031584 1.4017464 1.4493235 0.1580 M. danfossi 0.855844 1.3365128 0.6403563 0.5270 M. margotmarshae 2.793752 1.3365128 2.0903292 0.0455 M. mamiratra 4.209783 1.3365128 3.1498261 0.0038

#14 Forest - mm (Intercept) 2.473560 0.4771137 5.184425 0.0000 Forest-humid 2.637683 0.8148268 3.237109 0.0027

#15 Clade - mm (Intercept) 5.111243 0.6589051 7.757176 0.0000 Clade-nw -2.332712 0.8605922 -2.710589 0.0107 Clade-w -3.501767 1.1412571 -3.068342 0.0044 Mmyo: M. myoxinus, Mbon: M. bongolavensis, Mrav: M. ravelobensis, Mdan: M. danfossi, Mmar: M. margotmarshae, Mmam: M. mamiratra. *: p <0.05, **: p<0.01, ***: p<0.001

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Table 3.10 Summary of decided conflicts Number of decided conflicts won by each male or female in each male-female or male-male dyad and resulting dominance relationships in all six species. Displayed are also the body mass differences between both dyad partners Dyad type Species Dyad No. of decided Ind.1 Ind.2ª p-value Dominance Mass differenceb no. conflicts (g) Male-female M. myoxinus 1 2 1 1 0.5 +1 M. myoxinus 2 2 2 0 0.239 -1 M. myoxinus 3 3 0 3 0.124 +1 M. myoxinus 4 1 1 0 0.5 -1 M. myoxinus 5 1 0 1 0.5 +7 M. myoxinus 6 1 0 1 0.5 0 M. ravelobensis 1 0 0 0 0 M. ravelobensis 4 14 0 14 <0.001 FD -2 M. ravelobensis 5 0 0 0 +3 M. ravelobensis 6 5 2 3 0.5 -1 M. ravelobensis 7 2 1 1 0.5 -6 M. ravelobensis 8 11 2 9 0.035 FD +5 M. bongolavensis 1 0 0 0 +1 M. bongolavensis 2 0 0 0 0 M. bongolavensis 3 4 0 4 0.066 -9 M. bongolavensis 4 4 4 0 0.066 -9

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M. bongolavensis 5 8 0 8 0.007 FD +4 M. bongolavensis 6 4 0 4 0.066 -2 M. danfossi 1 29 4 25 <0.001 FD -8 M. danfossi 2 1 0 1 0.5 +4 M. danfossi 3 43 1 41 <0.001 FD 0 M. danfossi 4 1 0 1 0.5 +12 M. danfossi 5 18 3 15 0.004 FD -2 M. danfossi 6 1 0 1 0.5 -6 M. margotmarshae 1 22 16 6 0.028 MD -2 M. margotmarshae 2 3 1 2 0.5 -12 M. margotmarshae 4 25 0 25 <0.001 FD +12 M. margotmarshae 5 144 2 142 <0.001 FD -1 M. margotmarshae 6 1 0 1 0.5 +8 M. margotmarshae 7 30 9 21 0.022 FD -11 M. mamiratra 1 201 5 196 <0.001 FD -14 M. mamiratra 2 47 1 46 <0.001 FD +2 M. mamiratra 3 51 3 48 <0.001 FD +2 M. mamiratra 4 85 4 81 <0.001 FD 0 M. mamiratra 5 302 4 298 <0.001 FD -6 M. mamiratra 6 131 10 121 <0.001 FD +3 Male1-male2 M. myoxinus 7 0 0 0 0

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M. myoxinus 8 0 0 0 -2 M. myoxinus 9 0 0 0 -2 M. myoxinus 10 1 1 0 0.5 +14 M. myoxinus 11 2 1 1 0.5 +4 M. myoxinus 12 0 0 0 -1 M. ravelobensis 2 12 9 3 0.074 -25 M. ravelobensis 3 4 3 1 0.5 +10 M. ravelobensis 9 5 2 3 0.5 -5 M. ravelobensis 10 4 4 0 0.066 +5 M. ravelobensis 11 0 0 0 -2 M. ravelobensis 12 0 0 0 0 M. bongolavensis 7 18 3 15 0.004 M2 -10 M. bongolavensis 8 10 9 1 0.013 M1 -4 M. bongolavensis 9 6 0 6 0.02 M2 -1 M. bongolavensis 10 0 0 0 -20 M. bongolavensis 11 28 19 9 0.044 M1 -17 M. danfossi 7 21 6 15 0.040 M2 +1 M. danfossi 8 1 1 0 0,5 +1 M. danfossi 9 15 3 12 0.019 M2 0 M. danfossi 10 15 10 5 0.151 -2 M. danfossi 11 0 0 0 -1

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M. danfossi 12 1 0 1 0.5 +1 M. margotmarshae 3 10 1 9 0.013 M2 +6 M. margotmarshae 8 1 0 1 0.5 -4 M. margotmarshae 9 56 46 10 <0.001 M1 +5 M. margotmarshae 10 2 1 1 0.5 -3 M. margotmarshae 11 8 8 0 0.006 M1 0 M. margotmarshae 12 7 5 2 0.5 -2 M. mamiratra 7 79 2 77 <0.001 M2 +4 M. mamiratra 8 0 0 0 +1 M. mamiratra 9 63 9 54 <0.001 M2 -15 M. mamiratra 10 8 5 3 0.361 +1 M. mamiratra 11 15 13 2 0.005 M1 +16 M. mamiratra 12 18 13 5 0.049 M1 +4 Ind.: number of conflicts won by each individual of the respective dyad, a: In male-female dyads individual 2 is always the female, b: Negative value: Ind. 1 lighter than Ind. 2 - positive value: Ind. 1 heavier than Ind. 2, p-value: result of Binomial test, Bold values: p < 0.05, FD = female dominance; MD = male dominance; M1 = male 1 dominant; M2 = male 2 dominant

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Chapter 4 - General discussion

Six mouse lemur species were studied across a geographical transect from western to northwestern Madagascar. This region spans a geographical distance of about 355 km and is subdivided by five large rivers into different so-called inter-river-systems (IRSs) (Figure 3.7). This region is ecologically diverse (ranging from dry deciduous forests to humid evergreen rainforests) and harbors a total of eight Microcebus species (Figure 2.1) belonging to four different clades. All study sites underwent seasonality of temperature and rainfall across the years, although seasonality is stronger in the dry forest than in the rainforest. Day-night fluctuations in temperatures increase and rainfall is generally limited to only some months of the year in the deciduous forests (Rina Evasoa et al., 2018) in contrast to the lowland rainforest where temperature fluctuations are less extreme and some precipitations can be observed during all months of the year. As environmental seasonality is typically linked to seasonal phenology and food availability (Thorén et al., 2011, Wright, 1999), reproductive seasonality was expected in all study species and markedly in those populations in deciduous forests.

Socioecological theory predicts that reproduction and social tolerance will be tightly linked to each other in animal societies for several reasons (Ciani et al., 2012, Kappeler and van Schaik, 2002). For example, potential mates have to meet and interact in the reproductive season in order to reproduce although both partners may have different interests outside this context (e.g., sexual conflict during mate choice). In any case, encounter rates between the sexes can be expected to be higher in the reproductive season than in the non-reproductive season. Moreover, intra-sexual competition between males for gaining access to females can be assumed to be higher during the reproductive season than during the non-reproductive season. Furthermore, females of many lemur species have been shown to be rather intolerant towards a male, which seems to depend on the season and other species-specific factors (Hohenbrink et al., 2016). In view of the close link between both aspects, reproduction and social tolerance, both were jointly analyzed in some depth in the study species and will be discussed separately subsequently.

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4.1 Reproductive plasticity in mouse lemurs

Reproductive schedules varied across Microcebus species during the study period. Reproductively active females were detected as early as June in M. mamiratra but only later (August – November) in the other species. Together with the data on male testes volume, the results presented here in suggest a relatively early start of breeding season in three species (M. mamiratra, M. sambiranensis, M. danfossi) and a relatively later start in the other species (M. bongolavensis, M. ravelobensis, M. murinus, M.rufus, M. myoxinus, M berthae, and M. lehilahytsara), although sparse data precluded conclusive statements.

The observed interspecific variation in breeding phenology could not be explained by single predictors and the results suggest that an interaction of phylogeny and ecology may best explain the patterns of reproductive activity across all 12 study species (see chapter 2). For example, the influence of phylogeny could well explain the similarities within clades and the differences in reproductive schedules between sympatric species belonging to different mouse lemur clades such as the species pair M. murinus and M. ravelobensis, both being found in northwestern Madagascar.

On the other hand, the results of this research indicate that ecology influences reproductive phenology of mouse lemurs. For example, two geographically separated populations of M. murinus (Kirindy, Ampijoroa) differed in reproductive schedules, suggesting high intraspecific reproductive plasticity in habitats that differ at the start and in the amount of yearly rainfall. Moreover, species inhabiting the humid lowland forests differed from species living in dry forests, showing less pronounced seasonal reproduction than any other mouse lemur species. This finding could be best explained with high plant productivity in their environments, promoted by high yearly rainfall and relatively high temperatures, which allow mouse lemurs to reproduce during a season where all other species are unable to.

Aseasonal reproduction is uncommon among lemurs and also in mouse lemurs (Figure 4.1). The distribution of aseasonal reproduction across the phylogeny of mouse lemurs suggests that this trait may have evolved only once within this clade, possibly in the most recent common ancestor of a clade including M. mamiratra, M. margotmarshae, M. sambiranensis and M. arnholdi, for which phylogenetic relationships are not well resolved if it already inhabited lowland humid forests. Alternatively, the three species inhabiting these

65 habitats (M. mamiratra, M. margotmarshae and M. sambiranens) may have independently expanded their reproductive windows when colonizing and speciating in favorable lowland habitats within the last 2.64 mya (million years ago) (Louis Jr and Lei, 2016, Olivieri et al., 2007). However, considering the sister groupe of Mirza also shown aseasonality is at the moment impossible to discard the possibility that this character was retained in M. mamiratra, M. margotmarshae, and seasonality evolved in the others species.

Beyond mouse lemurs, aseasonal reproduction has so far been reported for some species, e.g., Eulemur rubriventer: Tecot (2010), Mirza zaza: Rode‐Margono et al. (2015), Daubentonia madagascariensis: Sterling (1994) (Figure 4.1).

In this study, species extend their breeding season or change from seasonal to a less seasonal breeding pattern due to the much higher amount of monthly rainfall per year and the unlimited food supply and high plant productivity. Habitat differences and the availability of resources facilitates earlier mating and birthing seasons, even if the general onset of reproductive activity is still determined by photoperiod (Verme, 1965, Verme, 1969, van Schaik and van Noordwijk, 1985, Perret and Aujard, 2001). The correlation of rainfall pattern and food quality with the mating/ birthing event in less pronounced seasonal species supports this concept (Moe et al., 2007).

Regarding the existing literature, the evolution of aseasonality is influenced by several factors such as geographically climatic differences (dry vs humid forest) (van Schaik and van Noordwijk, 1985), adaptation to the food succession throughout the year (Strier et al., 2001, Wright, 1999), a long day with more than 12h threshold in the day length in a photoperiod (Perret and Aujard, 2001).

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Figure 4.1 Evolution of seasonality (in red) and aseasonality (in blue) reproduction pattern in lemur species, the six study species (*), all species for which not has been observed or those without necessity information (in black). The time-tree of Strepsirrhini represents the combined results of several studies, as compiled in (Hedges et al., 2006)

4.2 Social plasticity in mouse lemurs

The third chapter revealed variation in social tolerance (e.g., affiliation pattern) and in its consequences (e.g., aggression rates) for six mouse lemur species that were studied with a standardised social encounter paradigm.

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Whereas the joint use of space and the total number of physical contacts represented correlates of social tolerance among the dyad partners in the encounter experiments, aggression rates and the total number of agonistic conflicts represented the consequences of low social tolerance in a competitive situation (constrained space/one food source provided).

There was only weak support for the influence of phylogeny on social tolerance and its outcomes. Typically, the four species inhabiting the dry forests (M. myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi) showed very similar behavioral responses despite belonging to two different phylogenetic clades. In contrast, habitat type (dry vs humid forest) could explain some variation, in particular, in the male-male dyads, as they showed higher social tolerance but also higher aggression rates and more agonistic conflicts in the humid forest than in the dry forest. Partial support was also given to the influence of reproductive activity on social tolerance and its consequences, although the behavior of M. danfossi (active reproduction) did not always correspond to the behavior of two other reproducing species (M. margotmarshae and M. mamiratra). The differences between these three species may best be explained with ecological factors, as M. danfossi inhabits dry deciduous forests and may have been energetically more constrained due to living in highly seasonal dry forests, whereas the other two species inhabit the less seasonal lowland humid forests. The third chapter also revealed significant support for species differences that could not be directly explained by way of phylogeny, habitat or reproductive activity. For example, M. bongolavensis differed significantly from M. danfossi in the joint space use, and M. mamiratra differed from M. margotmarshae in the number of conflicts and in the number of female-dominant dyads. It was therefore concluded that only the interaction between the different factors can best explain the findings of this study.

Regarding ecological factors, some of the findings did not follow the expectations that were formulated at the outset. For example, species living in the resource-poor dry forests did not compete more strongly in this competitive context than species from the humid forests. The relatively high levels of social tolerance in these species were attributed to the energetic constraints that these species undergo during the lean season (Gould and Sauther, 2007).

The third chapter described the social interactions that can be observed during a standardized encounter situation in a cage setting. During the observation period (six days), two rather unfamiliar animals were confined to a limited space and it is clear that under these artificial conditions the animals interacted more than usual during their nocturnal activity period in the

68 forest. It can be asked whether and in which way the observed variations in social tolerance and agonistic behavior may then reflect differences in social structure and social relationships that are formed and maintained by these species under natural conditions. There are at least two possible ways in which these observations may be linked to the natural behavior of mouse lemurs in the forest: First, if animals behave more tolerantly towards members of the same or opposite sex, this may indicate that they are more likely to form diurnal sleeping groups. If this holds true, it could be predicted, for example, that males of M. margotmarshae may form sleeping groups with other males under natural conditions as they were observed significantly more often in the same cage compartment than M. ravelobensis, M. bongolavensis or M. danfossi. Hending et al. (2017b) observed that males of M. sambiranensis, which is closely related to M. mamiratra, shared sleeping sites with others males. Future studies will be needed to investigate this hypothesis.

The observed patterns of social tolerance and its consequences may also inform us about the quality of interactions that may develop when two unfamiliar animals meet in the forest at nighttime (e.g., during locomotion or at a food resource). Such encounters have previously been reported concerning M. ravelobensis: Weidt et al. (2004), M. murinus: Radespiel (2000b), Thorén et al. (2016) and from M. griseorufus: Génin (2008) and can be expected for all species that have overlapping home ranges (M. murinus: Radespiel (2000b), M. ravelobensis: Weidt et al. (2004), M. rufus: Atsalis (2000), M. berthae: Dammhahn and Kappeler (2005), M. griseorufus: (Génin, 2008), M.sambiranensis: Hending et al. (2017a). With regard to this study, it could be predicted, for example, that male-females dyads of M. bongolavensis or male-male dyads of M. margotmarshae may show more affiliative behaviors than M. danfossi or that male-female dyads of M. mamiratra should show more aggressive behaviors upon social encounters than M. myoxinus, M. ravelobensis, M. danfossi or M. bongolavensis (Table 3.3).

4.3 Plasticity in female dominance among mouse lemurs

Female dominance among lemurs is widespread but is still controversially debated in behavioral ecology. Previous studies on female dominance suggested an influence of several factors on this trait that may vary in relevance between species: age, (ancestral) habitat, seasonal food availability, reproductive activity and experience (Jolly, 1984, Hrdy, 1981, Dunham, 2008, Hohenbrink et al., 2015, Petty and Drea, 2015, Gould and Sauther, 2007).

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Female dominance was detected in some study species (see chapter 3) but was not uniform in its expression. For example, no evidence of female dominance was found in Microcebus myoxinus, rare cases of female dominance were detected in M. ravelobensis and M. bongolavensis; moderate female dominance (50% female-dominant dyads) was observed in M. danfossi and M. margotmarshae, and unambiguous female dominance was noted in M. mamiratra (Table 3.1, Figure 4.2).

We explored the influence of phylogeny, habitat and reproduction on the establishment of dominance between dyad partners. Neither phylogeny nor ecology explained the variation in social dominance in the study species (Table 3.3). However, female dominance varied according to female reproductive activity in the population. Species with reproductively active females had higher numbers of female-dominant dyads than those studied outside reproduction. These results support previous studies that suggested a link between the establishment of female dominance and reproductive challenges in lemurs (Ellis, 1995). One limitation of the present study, however, is that each species was only studied during a limited period, either within or outside the reproductive season. For further understanding of the underlying proximate mechanisms and the intraspecific plasticity in this trait, future studies would benefit from studying each of these species across the year, i.e., in both rainy and dry season periods with different energetic constraints.

Female dominance is a relatively common phenomenon in lemurs and in mouse lemurs (Figure 4.2). The distribution of female dominance across the phylogeny of mouse lemurs suggests that this trait is widespread in the genus and occurred in several ligneage, and could have been present in the most recent common ancestor of genus of Microcebus. Remarkably two species inhabiting in lowland humid forests (M. mamiratra, M. margotmarshae). In this phylogenetic tree (Figure 4.2), female dominance in the genus of Microcebus is preponderant of which: 8 out of 19 Microcebus species showed female dominance, 2out of 19 displayed no female dominance, and 9 out of 19 no study on social behavior has been performed.

Beyond mouse lemurs, female dominance has been reported so far in other nocturnal taxa species (Figure 4.2) such as Daubentonia madagascariensis: Rendall (1993), Avahi occidentalis: Ramanankirahina et al. (2011), Phaner furcifer which is not shown in the Figure 4.2 but found only in the literature by Schülke and Kappeler (2003), and in diurnal and cathemeral species, for example, Propithecus diadema: Pochron et al. (2003), Propithecus

70 tattersalli: Meyers (1995b), Propithecus verreauxi: Richard and Heimbuch (1975), Eulemur mongoz: Curtis and Zaramody (1999). In the present study, species expanded their dominance pattern (Ramanankirahina et al., 2011) or changed from no female dominance (Eichmueller et al., 2013), moderate and unambiguous female dominance due to the energetic demand of the female, as well as the rejection of the male in the mating context. Within the reproductive actively in female or inactive, even if competition of resources is still determined by resources availability and amount of rainfall (Wright, 1999, van Schaik and van Noordwijk, 1985).

Figure 4.2 Partial clade showing evolution of female dominance in lemurs, the six study species (*), in red species for which female dominance is reported; in black species for which no female dominance has been observed or those without necessity information. The time-tree

71 of Strepsirrhini represents the combined results of several studies, as compiled in (Hedges et al., 2006)

4.4 Implications for taxonomy

This thesis is relevant for future studies on the systematics, taxonomy and biogeography of mouse lemurs as the information of breeding phenology and sociality can be of key importance in this primate group. Additionally, it provides information which is necessary to improve programs for lemur monitoring, management and conservation.

4.5 Implications for conservation

Each of the six species studied is somehow confined between two adjacent rivers in a pattern conforming seven adjacent Inter-River Systems (IRS) restricted to a small range of forest from northwestern to Northern Madagascar (see Figure 3.7). Their whole life history is restricted to the forest. The survival of Microcebus spp. only depends on the forest, which provides not only necessary food and appropriate substrates for locomotion (Ganzhorn, 1988), but also appropriate shelters for daytime sleeping groups (Hending et al., 2017b). In order to ensure and protect the remaining populations, a rapid conservation plan is needed for all species (Mittermeier et al., 2010).

4.6 Outlook

This thesis documents, for the first time, the reproduction schedule in some little known mouse lemur species. This study revealed first evidence of interplay between evolutionary history and ecology in the evolution of mouse lemur social behavior. The findings suggest that intraspecific and interspecific variation and regulation of social tolerance are much more complex than previously thought and vary considerably across species. Thus, current ecological hypotheses are not sufficient to explain the complex relations between ecology, reproduction, evolutionary history and sociality in this primate radiation. In this regards, further data need to be collected to elucidate which factors might explain the apparent plasticity and repeated evolution of breeding phenology and social interaction patterns within mouse lemurs and in lemurs in general. Future studies should attempt to (1) measure the same set of variables across the entire year and explore additional species across the mouse lemur’s

72 phylogenetic tree, (2) assess the plasticity in behavioral interactions and its outcomes on more species in different reproductive states of these threatened species.

Chapter 5 - References for introduction and discussion

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Acknowledgments

Though the following thesis is an individual study, I could never have reached the heights or explored the depths therefore without the help, support, guidance and effort of many individuals. I would like to extend my sincere thanks to all of them.

I am especially indebted to my main mentor, Pr. Dr. Elke Zimmerman, for giving me the opportunity to realize my PhD project. She worked actively to provide me with the protected academic time to pursue this thesis. She guided me through my work, helped me with valuable support and installed in me the qualities of a good scientist. She was candidly honest with me and answered all of my questions with straightforward advice. Not only did she provide me with scientific support but also she showed huge patience, and gave great support and understanding in difficult times.

I would especially like to thank my second mentor, Pr. Dr. Ute Radespiel who helped me with her guidance, encouragement, support, suggestions and very constructive criticism. She contributed immensely to the evolution of my ideas and development of my project. Furthermore, she invested an enormous amount of time for me and taught me a great deal about scientific research during my study period.

I would like to thank my committee members: Prof. Dr. Elke Zimmerman, Prof. Dr. Ute Radespiel, PD. Dr. Heike Hadrys and Prof. Dr. Julia Ostner for their advice and finding time for me in their busy schedule. I feel very grateful to have them in my supervisory group.

I am grateful to Sönke von den Berg and Tjard Bergmann for their technical support. Furthermore, a big thank you also goes to the entire members of staff at the Institute of Zoology, TiHo for their great support, suggestions and very constructive criticism. They

84 contributed immensely to the evolution of my ideas in this project during every Friday Seminar.

I am grateful to Sarah Hohenbrink, Daniel Schmidtke, Sharon Kessler and Jennifer Wittkowski for their advice and help.

I would also like to thank my colleagues in the office whom I spent time with during the week: Anette Klein, Alida Hasiniaina and Julia Jenikejew for being friendly to me.

My thanks go to the University of Veterinary Medicine Hannover (TiHo), the Hannover Graduate School for Veterinary Pathobiology, Neuroinfectiology and Translational Medicine (HGNI) for financing two international conference attendances in Strasbourg, France and in Kenya. I also wish to thank the PhD Program secretaries for their advice and help during the PhD courses.

I would like to thank to the “Gesellshaft Für Primatologie (GFP)” for subsidising the Congress fees in Kenya.

I would like to express my gratitude to the German Academic Exchange Service (DAAD) for subsidizing my German language courses for three years and six months.

I would like to acknowledge and thank Hasinala Ramangason for reading the very first draft of chapter 2, Dr. Mialy Razanajatovo who read and commented on the general introduction of the thesis.

I would like to acknowledge and thank Tracy Jepkoech Cherogony and Claude Arreyngang Tabe for translating the abstract in german.

A special word of gratitude goes to Marina Scheumann who read, commented and finalized the formatting of this thesis, to Frances Sherwood-Brock for proof-reading the English of the final draft, to Ariel Rodriguez who read and commented on the General Introduction and Discussion

The field work in six localities would have been impossible without the support and assistance from many people.

My warmest thanks go to Rufford Small Foundation for funding my fieldwork through Alida Hasiniaina’s grant.

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I would like to take this opportunity to thank Pr. Jean François Rajaonarison and Dr. Romule Rakotondravony of the University of Mahajanga for helping to conduct the necessary field work.

I am particularly grateful to Pr. Solofo Rasoloharijaona and Pr. Blanchard Randrianambinina for their help, support and advice during my studies in Germany as well as during the field in Madagascar.

My greatest thanks go to the students Hasinirina A.S. Andriamendrikaja, Ursulla L.Z. Mahatoly, Sandra P. Ratsimbazafy, and Etangie Radelin for their assistance in the field. Furthermore, to Jean Dé Rakotoarimanana, Jean Arsène and Dadabe , Xavier, Janardana Hasina Razanadahy, Lahantsoa, Ben Said, Anjara Jean Joel, Anuar Aly, and Amady Saidaly, David, Etienne, Patrice, and Tsaraleha, Taoro, Justira, Beanjara and Mainty who helped in capturing the animals and in guiding me through the forest.

I would like to thank the DGF (Ministère De L’Environnement, de L’Ecologie et des Forêts de Madagascar), MNP (Madagascar National Parks), MAAF (Madagascar Aye-aye Foundation), Lokobe National Park, Ankarafantsika National Park and their staff for granting me permission to conduct my fieldwork.

Thanks go to my six study animals: Microcebus myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi, M. margotmarshae and M. mamiratra for putting up with me and my colleagues when studying their social behavior. I expect this research will lead to their protection as well as the protection of their habitat.

I was surrounded by very kind people during my entire stay in Germany.

I would like to express my gratitude to Frau Maritta Ledwoch and Johanna Kroll for their heartwarming welcome and for organizing an unforgettable event for international students, helping and encouraging me with my tough time (finding a room, dealing with the visa issue…..). I am very grateful for their kindness.

I would like to thank my many friends and colleagues.

I express deep and sincere gratitude to my best friend Alida Hasiniaina for being a great friend. We have been friends since I studied at Mahajanga University in Madagascar. I am happy to have become her best friend since I started my PhD course in Hannover in 2015. Living in a foreign country was easy because of her. She is more than a friend to me, she is

86 my family, and she is like my younger sister. We shared a lot of things (room, office, travel, attending conferences and congresses, happiness, sadness, anxiety….). Indeed, we also had the same supervisor. I would like to thank her for spending twelve months with me for the fieldwork, living in the forest in Madagascar, and in Germany during the entire PhD program. A big thank you to her for being a flexible face to my strict character. Her friendship aided me ethically and helped me to keep on working during good and harder times.

I am extremely grateful to the catering team (Alida Hasiniaina, Helena Teixiera, Tania Bosia, Ricardo Cossio, Malcolm Chapcott and Frederic kiene), to the shopping team (Alida Hasiniaina, Hanitra Rakotonirina, Ando Rakotoarison and Fano Ratsoavina), they all made me feel at home.

I would like to thank all the European Ikala Stem members (Ikala Science Technology Engineering & Mathematics)” for scientific exchange experimentation in terms of serving our country (Madagascar).

I would like to thank the enthusiastic generous and kind member of the Hannover International Bible Church (HIBC) for welcoming me into their family.

I would also like to thank the entire Poukna Hannover members for their special events which made me feel at home, such as Independence Day celebration, Christmas celebrations.

I would like to acknowledge with gratitude the support and love of my family - my parents, Razanadahy Benoit and Razafindranoro Marie, my sister, Razanadahy Seheno, my brother, Razadahy Hasina Janardana, my nephew, Mahavitiany Christiano and my husband, Razafimanampimahafaly Edmond Adain. They all kept me going in whatever I pursued and this thesis would not have been possible without them.

Last but not least, I would like to offer this endeavor to our Lord God Almighty for the wisdom He bestowed upon me as well as, the strength, peace of mind and good health in order to complete this project.

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AFFIDAVIT

I herewith declare that I autonomously carried out the PhD-thesis entitled “The evolution of social dominance in mouse lemurs (Microcebus spp.): the effect of sex and species on social interaction”

No third party assistance has been used.

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 following institution: Institute for Zoology, 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.

______[date], signature

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