Socio-Ecological Determinants of Movement Behaviour in Red-Tailed Monkeys (Cercopithecus Ascanius Schmidti)

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Socio-Ecological Determinants of Movement Behaviour in Red-Tailed Monkeys (Cercopithecus Ascanius Schmidti) Socio-ecological determinants of movement behaviour in red-tailed monkeys (Cercopithecus ascanius schmidti) Edward McLester Submitted in partial fulfilment of the requirements of Liverpool John Moores University for the degree of Doctor of Philosophy, September 2020 Contents Abstract pg. 5 Declaration pg. 6 Acknowledgements pg. 7 Author contributions pg. 8 Ch. 1 Introduction pg. 10 Group-living among primates pg. 10 Group-living as an adaptive response pg. 10 Drivers of group ranging pg. 11 Drivers of group cohesion at the individual level pg. 12 Bidirectional communication as a mechanism of spatial cohesion pg. 13 Inter-habitat and intra-specific variation in group-living behaviour pg. 15 Thesis outline pg. 16 Ch. 2 Food abundance and weather influence habitat-specific ranging patterns in pg. 26 forest- and savanna mosaic-dwelling red-tailed monkeys (Cercopithecus ascanius) Abstract pg. 27 Introduction pg. 27 Methods pg. 29 Study sites pg. 29 Data collection pg. 30 Data analyses pg. 32 Results pg. 34 Home range sizes pg. 34 Daily travel distances pg. 40 Hourly and daily travel distances in response to weather pg. 40 Daily travel distances and home range use in response to food pg. 40 abundance Discussion pg. 43 Home range sizes and DTD reflect food abundance pg. 43 Thermal constraints on travel distances pg. 44 Determinants of home range use pg. 45 Hominin adaptations to savanna mosaic environments pg. 46 Supplementary material pg. 56 Ch. 3 Thermal conditions constrain group movements and habitat use in forest- and pg. 71 savanna woodland-dwelling red-tailed monkeys (Cercopithecus ascanius) Abstract pg. 72 Introduction pg. 72 Methods pg. 76 2 Study sites & groups pg. 76 Data collection pg. 78 Data analyses pg. 79 Results pg. 82 Hourly temperatures and solar irradiance pg. 82 Hourly travel distance pg. 82 Temperatures during open vegetation use pg. 84 Solar irradiance during open vegetation use pg. 84 Intra-group variation in open vegetation use at Issa pg. 84 Discussion pg. 86 Thermal conditions in forest and savanna-woodland mosaics pg. 86 Temperature constrains travel speed across habitats pg. 86 Thermal tolerance in open vegetation pg. 86 Forest loss can cause long-lasting thermal heterogeneity pg. 88 Hominin responses to changing thermal conditions pg. 89 Supplementary material pg. 96 Ch. 4 Food availability influences strategies of intra-group cohesion in red-tailed pg. 108 monkeys (Cercopithecus ascanius) Abstract pg. 109 Introduction pg. 109 Methods pg. 111 Data collection pg. 111 Data analyses pg. 113 Statistical analyses pg. 114 Results pg. 116 Spatial cohesion in relation group travel speed pg. 116 Spatial cohesion in relation to focal and nearest neighbour age- pg. 118 sex class Spatial cohesion in relation to individual behaviour pg. 118 Discussion pg. 118 Individual spatial cohesion as an alternative to group travel pg. 118 Spatial cohesion reflects individual cost-benefit ratios pg. 120 Spatial dimensions of intra-group feeding competition pg. 121 Spatial cohesion and social foraging pg. 121 Supplementary material pg. 128 Ch. 5 Contact call acoustic structure reflects antiphony in a wild primate pg. 133 (Cercopithecus ascanius) Abstract pg. 134 Introduction pg. 134 Methods pg. 135 3 Data collection pg. 135 Data analyses pg. 137 Statistical analyses pg. 137 Results pg. 139 Model selection per acoustic parameter pg. 139 Modulating effect of preceding grunts pg. 139 Modulating effects of nearest neighbour age-sex class and group pg. 139 travel speed Discussion pg. 141 Supplementary material pg. 146 Ch. 6 Conclusions pg. 153 Environmental influences on movement behaviour pg. 153 Individual behaviour reflects socio-ecological interactions pg. 154 Paleoecological drivers of primate movement behaviour in the Plio- pg. 157 Pleistocene Applications of primate movement behaviour in conservation pg. 159 Limitations and future studies pg. 160 4 Abstract In group-living primates, costs and benefits of sociality are reflected in movement behaviour: where groups move in their environment, and how individuals maintain cohesive groups while moving. Establishing environmental and social determinants of movement behaviour reveals adaptive responses that characterise primate sociality. For primates in different habitats, intra-specific behavioural variation provides insight into ecological pressures that drive habitat-specific adaptive responses. I investigated how group ranging and two individual behaviours that mediate intra-group cohesion – spatial positioning and contact calling – relate to food availability, weather, and social contexts in red-tailed monkeys (Cercopithecus ascanius), a forest guenon that also lives in forest scarce savanna-woodland environments. I predicted food availability and weather would have stronger effects on ranging in more seasonal savanna mosaics than forests, and individuals would 1) adjust inter-individual distances in response to increased feeding competition, and 2) adjust contact call acoustic structure to maximise propagation when neighbours were further away. I collected behavioural and ecological data at Ngogo, Uganda, a predominantly forested habitat with small patches of secondary forest, and Issa, Tanzania, a woodland-dominated mosaic with thin strips of riparian forest. Larger home ranges sizes and longer travel distances at Issa reflected lower food availability and hotter temperatures than at Ngogo. Behavioural responses to thermal conditions in secondary forest and woodland suggested comparable environmental heterogeneity across sites at fine spatial scales. Ngogo monkeys increased inter-individual distances where food availability was low and when travelling slower. Individual cohesion indicates trade-offs between reducing feeding competition and social foraging. Ngogo monkeys also adjusted call structures to match expected propagation to conspecifics depending if neighbours produced preceding grunts (i.e. antiphony). Environmental and social drivers of intra-specific movement behaviour reveal adaptive behavioural responses through which primates maintain sociality. Habitat-specific behaviour in red-tailed monkeys also improves our understanding of adaptations in hominins distributed across similar vegetation gradients. 5 Declaration No portion of the work referred to in this thesis has been submitted in support of an application for another degree or qualification of this or any other university or other institute of learning. 6 Acknowledgements Research at Ngogo, Kibale National Park, Uganda was conducted with permission from the Uganda Wildlife Authority, the Uganda National Council for Science and Technology, and Makerere University Biological Field Station, and permission and support from Michelle Brown and the Ngogo Monkey Project (NMP). Assistance with logistics and data collection at the NMP was provided by Felix Othieno, Toni Dotterer, and Godfrey Asaba. Additional facilities and assistance were provided by David Watts, John Mitani, Kevin Langergraber, Sam Angedakin, and the Ngogo Chimpanzee Project (NCP). Vegetation density data and additional ranging data were collected by and used with permission from Michelle Brown and the NMP *. Phenology data were collected by and used with permission from David Watts, John Mitani, Kevin Langergraber, and the NCP and provided by Kevin Potts *. Geospatial data from the Uganda Biomass Study were provided by Sylvia Amsler *. Research at the Issa Valley, Tanzania was conducted with permission from Kigoma and Mpanda district governments, the Tanzania Wildlife Research Institute, the Tanzania Commission for Science and Technology, and permission and support from Alex Piel, Fiona Stewart and the Greater Mahale Ecosystem Research and Conservation (GMERC) Project. Vegetation density data collected by Yahya Abeid and phenology data and additional ranging data collected by the GMERC Project were used with permission from Alex Piel, Fiona Stewart, and the GMERC Project *. This PhD project was supervised by Alex Piel (lead) and Serge Wich, with extremely helpful feedback on manuscript revisions from Russell Hill and Nicola Koyama. Funding was provided by the American Society of Primatologists (2017 General Small Grant) and the School of Biological and Environmental Sciences at Liverpool John Moores University (LJMU). Ethical approval was granted by the Faculty of Science at LJMU (approval reference: AP_EMcL/2016-3). Chapter 2 is published in full as: McLester E., Brown M., Stewart F. & Piel A. (2019). Food abundance and weather influence habitat-specific ranging patterns in forest- and savanna mosaic- dwelling red-tailed monkeys (Cercopithecus ascanius). American Journal of Physical Anthropology. 170: 217-231. https://doi.org/10.1002/ajpa.23920 * see individual chapter Acknowledgements. 7 Author contributions Chapter 1 EM designed and wrote the manuscript. Chapter 2 EM designed the study, collected ranging data, analysed all data, and wrote the manuscript with edits from MB, FS, and AP. MB collected ranging and vegetation plot data. FS and AP collected ranging, vegetation plot, phenology, and weather station data. Chapter 3 EM designed the study, collected ranging, behavioural, and weather station data, analysed all data, and wrote the manuscript with edits from MB, FS, and AP. MB collected ranging and vegetation plot data. FS and AP collected ranging, behavioural, vegetation plot, phenology, and weather station data. Chapter 4 EM designed the study, collected ranging and behavioural data, analysed all data, and wrote the manuscript. MB collected
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