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The Diademed Sifaka (Propithecus Diadema) and the Indri (Indri Indri)

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The Diademed Sifaka (Propithecus Diadema) and the Indri (Indri Indri) Infant Development and Maternal Strategies in the Two Largest Lemurs: The Diademed Sifaka (Propithecus diadema) and the Indri (Indri indri). by Jody Suzanne Weir B.Sc., The University of British Columbia, 2002 M.Sc., Texas A&M University, 2007 A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY in Interdisciplinary Studies © Jody Suzanne Weir, 2014 University of Victoria All rights reserved. This thesis may not be reproduced in whole or in part, by photocopy or other means, without the permission of the author. ii SUPERVISORY COMMITTEE Infant Development and Maternal Strategies in the Two Largest Lemurs: The Diademed Sifaka (Propithecus diadema) and the Indri (Indri indri). by Jody Suzanne Weir B.Sc., The University of British Columbia, 2002 M.Sc., Texas A&M University, 2007 Supervisory Committee Dr. Lisa Gould, Department of Anthropology Co-Supervisor Dr. Barry Glickman, Department of Biology Co-Supervisor Dr. Steig Johnson, Department of Anthropology, University of Calgary Committee Member iii ABSTRACT Supervisory Committee Dr. Lisa Gould, Department of Anthropology Co-Supervisor Dr. Barry Glickman, Department of Biology Co-Supervisor Dr. Steig Johnson, Department of Anthropology, University of Calgary Committee Member At least half of the world’s primate species are currently threatened with extinction. Slow life histories combined with rapid habitat loss and hunting in recent years has heightened the extinction risk for many species, including the two largest extant lemurs, the diademed sifaka (Propithecus diadema) and the indri (Indri indri). Both species belong to the taxonomic family Indriidae, have similar adult weights, and occur in sympatry in certain areas of the montane rainforests of eastern Madagascar. Both species are adapted for folivory however I. indri spend considerably more time feeding on leaves than do P. diadema resulting in several energy-saving adaptations in I.indri. In this dissertation, I explore infant development and maternal strategies of these critically endangered primates with the goal of increasing our knowledge of reproduction and ontogeny in both species. Although previous studies have elucidated key differences in adult behaviour, there is a dearth of information on infants and lactating females in either of these two species. Between June and December of 2011 and 2012, I collected continuous time focal animal data, in Maromizaha forest, to examine behavioural patterns of 12 infants and their mothers from 0 – 33 weeks. In addition, I developed a framework to define and quantify the weaning process and facilitate comparisons across different species and studies. P. diadema infants developed feeding competency and independent locomotion faster than did I. indri infants however both species were consistently feeding iv independently more than they were suckling by week 20. The process of feeding ontogeny in I. indri was likely accelerated by coprophagy, as all infants of this species consumed their mother’s feces regularly from 10 – 15 weeks old. Lactating females of both species spent more time feeding in mid-lactation when maternal investment was the highest. The prolonged inter-birth interval in I. indri is suggested as another adaptation that reduces energetic expenditures. In addition, the protracted period of close contact with their mother may offer infant I. indri more time for social learning of the mother’s diet and the group song and for developing competency in vertical clinging and leaping without a tail for balance and support. v TABLE OF CONTENTS SUPERVISORY COMMITTEE............................................................................ii ABSTRACT ...........................................................................................................iii TABLE OF CONTENTS .......................................................................................v LIST OF TABLES .................................................................................................vii LIST OF FIGURES................................................................................................ix ACKNOWLEDGMENTS......................................................................................xiv DEDICATION .......................................................................................................xvii CHAPTER ONE INTRODUCTION .....................................................................................................1 1.1 Extinction risk, Madagascar, and the challenges facing lemur conservation.1 1.2 Conservation strategies for lemurs threatened with extinction......................5 1.3 Infant Development in Primates ....................................................................8 1.4 Study Species 1– Diademed Sifaka (Propithecus diadema)..........................13 1.5 Study Species 2– Indri (Indri indri)...............................................................15 1.6 Study Site.......................................................................................................18 1.7 Objectives and Significance...........................................................................23 1.8 References......................................................................................................25 CHAPTER TWO PHASES OF WEANING, EARLY ONTOGENY AND SURVIVAL OF DIADEMED SIFAKA (Propithecus diadema) INFANTS AT MAROMIZAHA FOREST 2.1 Introduction....................................................................................................34 2.2 Methods..........................................................................................................45 2.3 Results............................................................................................................50 2.4 Discussion......................................................................................................63 2.5 References......................................................................................................76 CHAPTER THREE DIET, COPROPHAGY AND PHASES OF FEEDING ONTOGENY OF INDRI (Indri indri) INFANTS AT MAROMIZAHA FOREST 3.1 Introduction....................................................................................................85 3.2 Methods..........................................................................................................94 3.3 Results............................................................................................................99 3.4 Discussion......................................................................................................114 3.5 References......................................................................................................125 CHAPTER FOUR VARIABLES AFFECTING INFANT DEVELOPMENT IN THE TWO LARGEST LEMURS 4.1 Introduction....................................................................................................135 4.2 Methods..........................................................................................................142 vi 4.3 Results............................................................................................................146 4.4 Discussion......................................................................................................154 4.5 References......................................................................................................161 CHAPTER 5 VARIABLES AFFECTING MATERNAL STRATEGIES IN THE TWO LARGEST LEMURS 5.1 Introduction....................................................................................................169 5.2 Methods..........................................................................................................182 5.3 Results............................................................................................................185 5.4 Discussion......................................................................................................197 5.5 References......................................................................................................204 CHAPTER 6 CONCLUSION..........................................................................................................212 6.1 Summary........................................................................................................212 6.2 Future Directions ...........................................................................................219 6.3 References......................................................................................................221 APPENDICES APPENDIX I .............................................................................................................228 APPENDIX II ............................................................................................................229 APPENDIX III...........................................................................................................230 APPENDIX IV...........................................................................................................231 vii LIST OF TABLES CHAPTER ONE Table 1.1 Characteristics of four field sites where studies of Indri indri and Propithecus diadema have previously taken place............................13 CHAPTER TWO Table 2.1 Ecology and infant developmental schedules in six species of wild lemur.................................................................................................. 37 Table 2.2 Mother-infant dyads within four groups of P. diadema over two successive
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