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Lemurs on a Sinking Raft? Lemurs on a sinking raft? The ballast of anthropogenic disturbances Iris I. de Winter Thesis committee Promotor Prof. Dr H.H.T. Prins Professor of Resource Ecology Wageningen University & Research Co-promotors Dr I.M.A. Heitkönig Assistant professor, Resource Ecology Group Wageningen University & Research Dr W.F. van Hooft Assistant professor, Resource Ecology Group Wageningen University & Research Other members Prof. Dr M. Naguib, Wageningen University & Research Prof. Dr E.H.M. Sterck, Utrecht University Dr N. Tagg Nama, Conservation Royal Zoological Society of Antwerp, Belgium Dr E. Meijaard, The University of Queensland, Australia This research was conducted under the auspices of the C.T. de Wit Graduate School for Production Ecology and Resource Conservation (PE&RC) Lemurs on a sinking raft? The ballast of anthropogenic disturbances Iris I. de Winter Thesis submitted in fulfilment of the requirements for the degree of doctor at Wageningen University by the authority of the Rector Magnificus Prof. Dr A.P.J. Mol, in the presence of the Thesis Committee appointed by the Academic Board to be defended in public on Monday 11 June 2018 at 11 a.m. in the Aula. Iris I. de Winter Lemurs on a sinking raft? The ballast of anthropogenic disturbances 266 pages. PhD thesis, Wageningen University, Wageningen, the Netherlands (2018) With references, with summaries in English, Dutch, Malagasy, and French ISBN 978-94-6343-288-7 DOI 10.18174/449281 PREFACE Wild primates are fascinating creatures that occupy a special place in the hearts of people around the globe. The clade of lemurs evolved in isolation, exclusively on the island of Madagascar, yet the magnitude of its behavioural and morphological diversity rivals that of the monkeys and apes found elsewhere in the world. One truly feels fascinated when near these agile tree dwellers as they serenely warm up in the sun, groom each other, or move through the lush vegetation, observing us observing them with a mirrored curiosity vividly apparent in their striking eyes. It is worrisome to imagine a world without these charming animals; but, with a combination of ongoing research, clear communication, and the development and implementation of effective conservation measures, we may not have to. 5 CONTENTS Chapter 1: General Introduction 9 Chapter 2: Anthropogenic disturbance effects remain visible in forest structure, but not in lemur abundances 27 Chapter 3: The coexistence of two congeneric lemur species 51 Chapter 4: Occupancy strongly influences faecal microbial composition of wild lemurs 77 Chapter 5: Effects of seasonality and previous logging on faecal helminth-microbiota associations in wild lemurs 101 Chapter 6: Determining Mhc-DRB profiles in wild populations of three congeneric true lemur species by non-invasive methods 125 Chapter 7: Synthesis: How to keep the raft afloat? 145 Bibliography 171 Summaries 219 Acknowledgements 237 Short biography 251 Publications 255 PE&RC Training and Education statement 259 7 CHAPTER 1 GENERAL INTRODUCTION Like all of the earth’s natural ecosystems, tropical forests are influenced by a wide range of anthropogenic and natural impacts (Barlow et al., 2016). Anthropogenic disturbances to the natural environment date back to early human occupation in the tropics. Especially when humans started using fire, about 1.8 million years ago (mya), landscape modification and biotic adjustments became more intense (Vié et al., 2009). The shift from hunting-gathering to farming was one of the most important factors that has sparked land conversion and modification (Goudie, 2013). Given the tendency of humans to directly and often considerably alter and impact the environment, nearly all currently-existing forests, including tropical forests, have experienced anthropogenic forest exploitation (Bicknell et al., 2015). Although tropical forests form less than 10 percent of the world’s land area, half of all animal and plant species and even 90 percent of all nonhuman primates that are known today rely on these forests for their subsistence (Mayaux et al., 2005; Whitmore et al., 1992). Because of ongoing loss of tropical forests, all these species have become vulnerable, and population densities and distributions of many species are in decline (Chapman et al., 2007; Cowlishaw and Dunbar, 2000; Fashing, 2002). Human interferences with the environment are not limited to mainland forests. Human discovery of and arrival on numerous remote islands within the world’s oceans has drastically changed many island ecosystems. Due to their isolation, unique geology, and climate regimes, islands are often home to a diverse array of ecosystems that host rare and endemic flora and fauna (Yoder and Nowak, 2006). In addition to anthropogenic impacts, local natural disturbances of tropical forests have occurred over large geographical time scales. These disturbances range from small-scale events, such as tree-falls, to larger-scale processes, such as erosion, fire, and annual flooding. Tropical forests have always been highly impacted by other natural phenomena: geological events (e.g., earthquakes, landslides, and volcanic eruptions), atmospheric events (e.g., tropical cyclones, droughts, and lightning), climatic variations (e.g., ice ages and sea level fluctuations), and other hazards (e.g., disease epidemics and insect infestations). In addition, environmental circumstances, like soil and climate conditions as well as topography, influence the makeup and function of forest ecosystems (reviewed in Chazdon 2003). Anthropogenic disturbances and natural challenges interact with each-other in complex ways and together shape the ecosystems in which many unique plant and animal species reside. This chapter forms a general introduction that sets the scene by presenting the 9 CHAPTER 1 theoretical framework of this thesis, including an overview of the available literature. I 10 outline the scope; introduce the aim, main questions, and hypothesis; and provide the study design, including a biological background of the study species and information on the geographic locations. THE ISLAND OF MADAGASCAR Despite its proximity to Africa, the island of Madagascar has a very different biotic and human history than that of the mainland. Continental drift led to its isolation and, together with India and Antarctica, Madagascar split from the Africa-South America landmass approximately 165 mya, reaching its current position around 120 mya (Coffin and Rabinowitz, 1992). The estimated continental breakup of Madagascar and India was 88 mya (Storey et al., 1995). Over millions of years, a number of distinct biomes have developed on the island. On a geologic timescale, transportation via rafts of floating debris has played an important role in dispersal of organisms around the globe, especially for non-swimming and non-flying organisms (Heatwole and Richard, 1972). For example, New World Monkeys originated in Africa and rafted during the Eocene to South America (Bond et al., 2015). Tropical storms and flooding events are known to rip away floating lumps of earth, complete with living vegetation and micro-ecosystems (Simpson, 1940). Vertebrate colonisation of Madagascar most likely occurred via this type of dispersal, on floating rafts of vegetation across the ocean (Ali and Huber, 2010). This theory also holds for lemurs, a clade of endemic Strepsirrhine primates that arrived on the island between 60 and 50 mya (Yoder and Yang, 2004, Box 1.1). During this geological period, both Madagascar and Africa were located approximately 1650 kilometres south of their present positions and ocean currents ran in eastern direction from Africa towards Madagascar (Ali and Huber, 2010). Natural rafts for a lemur ancestor could therefore have been formed from vegetation lining rivers on the east coast of Africa -for example, from riverbanks of the Zambezi or from the shoreline of northeastern Mozambique and Tanzania- and transport should have been towards the northwest coast of Madagascar (Stankiewicz et al., 2006). By floating on such rafts of vegetation, a lemur ancestor, possibly a single pregnant female, migrated from mainland Africa, transported by ocean currents across the approximately 400 km wide Mozambique Channel, and stranded on the enormous ’raft’ called Madagascar (Ali and Huber, 2010). About 40 mya, the currents gradually changed southwards, thereby putting an end to any further oceanic transport and isolating Madagascar and its inhabitants from other landmasses (Ali and Huber, 2010). Lemurs evolved in isolation, independent of competition from monkeys, apes, or other ecologically-competitive large-bodied mammals (Yoder and Nowak, 2006). Madagascar varies widely in climate, seasonality, GENERAL INTRODUCTION and geology across the island (Fig. 1.1, Yoder & Nowak 2006); to avoid competition with conspecifics, lemur populations were forced to limit niche overlap as much as 11 possible, driving them into Madagascar’s numerous environmental niches. This led to the adaptive radiation of more than a hundred different species (Yoder and Yang, 2004), representing 29 percent of all primate families and 20 percent of the genera and species that are known today (Table 1.1, Bowman et al. 2018). Lemurs are one the most diverse and geographically isolated groups of primates in the world. They are only found on Madagascar, and are recognised as keystone species in some of the most endemic and threatened ecosystems in the world (Schwitzer, 2014). Box 1.1 The lemur clade. Lemurs - Kingdom: Animalia, Phylum: Chordata, Class:
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