Behavioral and Feeding Ecology of a Small-bodied Folivorous Primate (Lepilemur leucopus) Dissertation for the award of the degree “Doctor rerum naturalium” (Dr. rer. nat.) of the Georg-August-Universität Göttingen within the doctoral program Biology of the Georg-August University School of Science (GAUSS) submitted by Iris Dröscher from Scheifling, Austria Göttingen 2014 Thesis Committee: Prof. Dr. Peter M. Kappeler, Department of Sociobiology and Anthropology, Georg- August-Universität Göttingen, Behavioral Ecology and Sociobiology Unit, German Primate Center GmbH Prof. Dr. Eckhard W. Heymann, Department of Sociobiology and Anthropology, Georg- August-Universität Göttingen, Behavioral Ecology and Sociobiology Unit, German Primate Center GmbH Members of the Examination Board: Reviewer: Prof. Dr. Peter M. Kappeler Second Reviewer: Prof. Dr. Eckhard W. Heymann Further members of the Examination Board: Dr. Claudia Fichtel, Behavioral Ecology and Sociobiology Unit, German Primate Center GmbH Prof. Dr. Julia Ostner, Primate Social Evolution Group, Courant Research Centre Evolution of Social Behavior, Georg-August-Universität Göttingen Dr. Oliver Schülke, Primate Social Evolution Group, Courant Research Centre Evolution of Social Behavior, Georg-August-Universität Göttingen Dr. Dietmar Zinner, Cognitive Ethology Laboratory, German Primate Center GmbH Date of the oral examination: 12 December 2014 CONTENTS SUMMARY ………………………………………………………………………………1 ZUSAMMENFASSUNG …………………………………………………………………3 GENERAL INTRODUCTION …………………………………………………………...5 CHAPTER 1 ……………………………………………………………………………..19 Defining the low end of primate social complexity: the social organization of the nocturnal white-footed sportive lemur (Lepilemur leucopus) CHAPTER 2 …………………………………………………………………………..…45 Competition for food in a solitarily foraging folivorous primate (Lepilemur leucopus)? CHAPTER 3 ……………………………………………………………………………..71 Maintenance of familiarity and social bonding via communal latrine use in a solitary primate (Lepilemur leucopus) CHAPTER 4 ……………………………………………………………………………105 Nutritional consequences of folivory in a small primate: effects of season and reproduction on nutrient balancing GENERAL DISCUSSION ……………………………………………………………..135 REFERENCES …………………………………………………………………………147 APPENDICES ………………………………………………………………………….187 ACKNOWLEDGMENTS ……………………………………………………………...189 CURRICULUM VITAE ……………………………………………………………….191 DECLARATION ………………………………………………………………………192 Summary SUMMARY Small-bodied folivorous primates are rare because processing leaves often requires extensive gut adaptations and lengthy retention times for fiber fermentation. However, Lepilemur leucopus (white-footed sportive lemur) persists on a folivorous diet despite small body size (<1kg). To improve our knowledge about how small-bodied folivores adapt their behavioral and dietary strategies to satisfy their nutritional needs, I aimed to investigate how extrinsic (i.e. food quantity and quality) and intrinsic (i.e. reproductive state) factors influence foraging strategies, food choices and social relationships. I collected data on activity patterns, feeding behavior, social interactions and ranging behavior in a spiny forest population of L. leucopus at Berenty Reserve, Madagascar, over a complete annual cycle. I determined habitat structure and phenology of the spiny forest and collected foods for chemical analyzes of nutritional content. There was no consistent evidence that the seasonal decrease in food quantity had a major impact on feeding behavior or social interactions in L. leucopus, presumably due to its low dietary selectivity and reliance on the most common food species, and any feeding stress may have been more related to food quality than quantity. In more particular, dietary protein may have been in limited supply as L. leucopus prioritized protein over non-protein intake across seasons and reproductive stages. As changes in activity patterns and social interactions were unrelated to food quantity, bottom-up processes seem to be less important than top-down processes in shaping the social system of L. leucopus. The findings also support the idea that quantitative food shortage during the dry season may be subordinate to leaf quality as a selection pressure on folivorous primate populations. 1 Summary 2 Zusammenfassung ZUSAMMENFASSUNG Kleine blattfressende Primaten sind selten, da die Verarbeitung von Blättern oft umfangreiche Anpassungen des Verdauungsapparates und lange Retentionszeiten für die Fermentierung der Blattfasern erfordert. Dennoch basiert die Nahrung von Lepilemur leucopus (Weißfuß-Wieselmaki) auf Blättern trotz kleinem Körpergewichts (<1 kg). Um unser Verständnis darüber voranzutreiben wie kleine Blattfresser ihre Verhaltensstrategien anpassen um ihre Nahrungsbedürfnisse zu stillen, beabsichtigte ich zu untersuchen wie extrinsische (i.e. Nahrungsquantität und -qualität) und intrinsische Faktoren (i.e. Fortpflanzungsstatus) Strategien der Nahrungssuche, Nahrungswahl und soziale Interaktionen beeinflussen. Ich sammelte Daten bezüglich Aktivitätsmuster, Fressverhalten, sozialer Interaktionen und Streifverhalten in einer Population von L. leucopus in Berenty Reserve (Madagaskar) über einen kompletten Jahreszyklus. Ich erhob Daten zur Habitatstruktur und Phänologie des Dornenwaldes und sammelte Blattproben für die chemische Analyse des Nährstoffgehaltes. Es gab keine eindeutigen Anhaltspunkte, dass die saisonale Abnahme in der Nahrungsverfügbarkeit einen beträchtlichen Einfluss auf Fressverhalten oder soziale Interaktionen in L. leucopus hatte, vermutlich aufgrund der geringen Nahrungsselektivität und der Nutzung der am häufigsten im Wald vorkommenden Pflanzenarten, und Nahrungsstress stand wahrscheinlich eher mit Nahrungsqualität als -quantität in Verbindung. Nahrungsprotein scheint nur begrenzt zur Verfügung gestanden zu haben, da L. leucopus Protein- gegenüber nicht-Protein-Aufnahme über Jahreszeiten und Reproduktionsstadien hinweg priorisierte. Da Veränderungen hinsichtlich Aktivitätsmuster und sozialer Interaktionen nicht im Zusammenhang mit Nahrungsknappheit standen, scheinen Bottom-Up-Prozesse weniger wichtig als Top-Down-Prozesse für die Formgebung des sozialen Systems von 3 Zusammenfassung L. leucopus zu sein. Die Ergebnisse unterstützen außerdem die Idee, dass quantitative Nahrungsknappheit während der Trockenzeit eine untergeordnet Rolle gegenüber Blattqualität als Selektionsdruck für blattfressende Primatenpopulationen spielt. 4 General Introduction GENERAL INTRODUCTION Nutrition is the basis for all life processes as it delivers energy for maintenance, growth and reproduction. As diet is related to almost all aspects of behavior, morphology, and physiology, it is a central component of a species’ biology. Moreover, a species’ feeding ecology relates to its life history, population dynamics, habitat requirements, and patterns of sociality (Robbins and Hohmann 2006). Furthermore, studies of the chemical basis of food choice further our understanding of foraging strategies and dietary decisions (Whiten et al. 1991), of the ecological basis of variation in social organization (Byrne et al. 1993), and of the determinants of animal abundance (Chapman et al. 2002). In general, the rate at which an individual can acquire energy and nutrients depends on the quantity and quality of the available food resources, and foraging behavior can be considered successful only if the diet obtained provides sufficient amounts of energy and nutrients to fulfill the energetic and nutritional requirements of the forager (Oftedal et al. 1991). The rate of energy gain and nutrition of an individual is influenced by several factors such as a.) species-specific diet, b.) seasonal variation in the quantity, quality and distribution of food resources, c.) sex-specific differences in energetic needs due to differing costs of reproduction and d.) the presence of other individuals that compete for the same food resources. In this general introduction, I will provide more details on each of these factors. Subsequently, I will outline why the white-footed sportive lemur (Lepilemur leucopus) constitutes a suitable study species. Finally, I will highlight which aspects of the behavioral and feeding ecology of L. leucopus I explored in each chapter of this thesis and which approaches I used to do so. 5 General Introduction Species-specific diet Primates are able to exploit a wide range of food sources such as fruits, leaves, flowers, seeds, insects or gums. Therefore, individual species are often referred to as predominantly frugivorous, insectivorous, gummivorous or folivorous according to the dominant type of food, and dietary adaptations can be related to the structural and biochemical features of their food sources (Lambert 1998). Although large animals have higher absolute metabolic requirements than small animals, they actually require less energy intake per unit of body weight. Therefore, large animals are able to subsist on abundant low-quality foods, whereas small animals tend to concentrate on relatively rare foods of high quality (Gaulin 1979). The major food type of small primates tends to be invertebrates, whereas fruits, seeds or gum are usually the principal foods of medium- sized species. In contrast, larger species rely on leaves as the major food source (Hladik 1979). The diet of insectivorous primates is high in protein, energy and is easy to digest (Schmidt-Nielsen 1997). However, insects are often scarce food items as they are small in size, very seasonal and less abundant than leaves and