Effects of the social environment on the behaviour and fitness of a territorial squirrel by Erin Rose Siracusa A Thesis presented to The University of Guelph In partial fulfillment of requirements for the degree of Doctor of Philosophy in Integrative Biology Guelph, Ontario, Canada © Erin Rose Siracusa, September 2018 ABSTRACT EFFECTS OF THE SOCIAL ENVIRONMENT ON THE BEHAVIOUR AND FITNESS OF A TERRITORIAL SQUIRREL Erin Rose Siracusa Advisor: University of Guelph, 2018 Dr. Andrew G. McAdam Most organisms interact with conspecifics and therefore have a social environment. While it is understood that variation in the composition of this social environment can have important consequences for gregarious species, solitary, territorial species may also live in socially complex environments where the composition of neighbouring conspecifics can directly influence time and energy spent on territory defence. The importance of the social environment for solitary species is, however, poorly understood. In this thesis, I combined behavioural observations, field experiments, and long-term data analysis from a population of North American red squirrels (Tamiasciurus hudsonicus) to explore the effects of the social environment on the territorial dynamics, behaviour and fitness of an ‘asocial’ species. In particular, I looked at two aspects of the social environment that were likely to have important effects on territorial species: familiarity and relatedness with neighbours. In my first chapter, I established that squirrels living in social neighbourhoods with high average familiarity faced reduced risk of intrusion and cache pilferage from conspecifics, providing evidence of the ‘dear- enemy’ phenomenon in red squirrels. In Chapter 2, I experimentally demonstrated that red squirrel ‘rattle’ vocalizations serve an important territorial defence function by deterring conspecifics from intruding. In Chapter 3, I found that red squirrels respond to changes in their social environment by adjusting their behaviour in a manner that reduces the costs of territoriality: in familiar social neighbourhoods red squirrels reduced their rattling rates and increased the proportion of time spent in nest. Finally, in Chapter 4, I used 21 years of data to show that living near familiar neighbours has substantial fitness benefits, increasing annual reproductive success and survival in both male and female squirrels. Collectively my thesis contributes to our broader understanding of the importance of the social environment for ‘asocial’ species and provides evidence that interactions between territorial individuals are not strictly competitive but can also be cooperative in nature. In particular, mutualistic interactions, rather than kin-selection, were important in mitigating conflict and enhancing fitness. Studying social interactions in asocial animals may, therefore, provide important insights into the mechanisms driving the evolution of social systems. iv DEDICATION To my parents, Jeanne Beno and Alan Siracusa, who first taught me the names of wild things, who gave me acres of woodland to romp, who let me wade in the mud after salamanders and tadpoles, and who pulled me from my bed at unreasonable hours of the morning to see the sun rise. To my parents, who taught me a deep respect for all living things and instilled in me an unsurpassed love for the natural world. It is because of you that I am a biologist today. v ACKNOWLEDGEMENTS My thanks must first and foremost go to my advisor, Andrew McAdam, and to the members of the McAdam lab, Julia Kilgour, Simon Denomme-Brown, Jack Robertson, David Fisher, Maggie Bain, Shelby Bohn and Sarah Guindre-Parker, who have been my academic family for the past 5 years. I consider myself extraordinarily lucky to have landed in a graduate program where I have had the opportunity to work with such supportive, caring, intelligent and creative colleagues on a daily basis. You have each been an inspiration to me, and have taught me not only how to be a better scientist but also a better human being. It is my most sincere hope that every graduate student has the opportunity to work with such a tremendous advisor and lab group. To my incredibly hard-working and dedicated field assistants – Jack Robertson, Sam Sonnega, Marta Thorpe, and Yuqing Sun – without you none of this research would have been possible. Thank you for your quick thinking, your laughter, and your unending supply of wit that got me through even the toughest days in the field. I am indebted to you for helping make me a better mentor. To my KRSP family, who helped to make the fifteen months that I spent at Squirrel Camp some of the best of my life, especially Lisa Bidinosti, Naomi Louchouarn, Sarah Nason, Alec Robetaille, Sarah Westrick and Marina Morandini. A very special thanks to Emily Studd, who first taught me the art of squirrelling and who has been an indomitable source of friendship and laughter ever since. I am grateful to all of my collaborators and mentors, including my committee members, Ryan Norris, Elena Choleris, and Beren Robinson; the KRSP principle investigators, Stan Boutin, Murray Humphries, Ben Dantzer, Jeffrey Lane; and our bioacoustics expert, Dave Wilson. These folks have devoted their time and energy to providing feedback on experimental design, assisting with data analysis, listening to presentations, and commenting on manuscripts. Their efforts have enhanced the quality of my work and made me a better scientist. I am humbled and grateful to have had the opportunity to work with such an esteemed group. vi I owe a special thank you to Erika Barthelmess who changed my life and first set me down this path when she agreed to be my undergraduate advisor. When I couldn’t decide if I wanted to be a writer or a biologist, Erika encouraged me to be both, and I am a better scientist for it. Her teaching and mentorship have shaped the professor that I hope to one day become. Finally, and most importantly, I am deeply thankful for my partner, Josh LeBlanc, who, despite completing a PhD of his own and taking on extensive teaching responsibilities in the course of his degree, has never once wavered in his support. In the course of 5 years together we have overcome three surgeries and a major concussion, we have thoroughly confused Canadian border agents by swapping out our vehicle at least four times, and somehow managed to wrangle a queen-sized mattress into fitting a full-size bed frame. You have dealt with my prolonged absences in the field, have seen me through tears of loneliness, sorrow, and frustration and somehow, through all of it, have remained patient, supportive, and kind. I am deeply indebted to you for your love and support throughout this process. This research would not have been possible without the support of the Champagne and Aishihik First Nations, especially Agnes MacDonald and her family, who have allowed us for the past 30 years to study red squirrels on their traditional territory. My research was generously supported by a variety of funding sources including an Ontario Trillium Scholarship, Grants-in-Aid of Research from the American Society of Mammalogists and the Arctic Institute of North America, an Elgin Card Scholarship in Terrestrial Zoology from the University of Guelph, and the Natural Sciences and Engineering Research Council of Canada. vii TABLE OF CONTENTS Abstract ........................................................................................................................................... ii Dedication ...................................................................................................................................... iv Acknowledgements ......................................................................................................................... v Table of Contents .......................................................................................................................... vii List of Tables ................................................................................................................................. ix List of Figures ................................................................................................................................. x Prologue ......................................................................................................................................... xi Chapter Publications and Author Contributions .......................................................................... xvi Chapter 1: Familiarity With Neighbours Affects Intrusion Risk In Territorial Red Squirrels ....... 1 Abstract ....................................................................................................................................... 1 Introduction ................................................................................................................................. 1 Methods....................................................................................................................................... 6 Results ....................................................................................................................................... 13 Discussion ................................................................................................................................. 14 Tables ........................................................................................................................................ 21 Figures......................................................................................................................................