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Tamiasciurus Hudsonicus) University of Calgary PRISM: University of Calgary's Digital Repository Graduate Studies The Vault: Electronic Theses and Dissertations 2014-04-28 Patterns and Consequences of Parasitism in North American Red Squirrels (Tamiasciurus hudsonicus) Patterson, Jesse Patterson, J. (2014). Patterns and Consequences of Parasitism in North American Red Squirrels (Tamiasciurus hudsonicus) (Unpublished doctoral thesis). University of Calgary, Calgary, AB. doi:10.11575/PRISM/27274 http://hdl.handle.net/11023/1436 doctoral thesis University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca UNIVERSITY OF CALGARY Patterns and Consequences of Parasitism in North American Red Squirrels (Tamiasciurus hudsonicus) by Jesse Eric-Henry Patterson A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY DEPARTMENT OF BIOLOGICAL SCIENCES CALGARY, ALBERTA APRIL 2014 © Jesse Eric-Henry Patterson 2014 Abstract Parasites are ubiquitous in nature and, by definition, impose harm on their hosts. The degree of harm is dependent upon many factors, such as co-evolutionary history, host immunity, and the magnitude of infection. Hosts must balance the costs of parasitism with investment in growth, development, and reproduction in order to maximize their fitness. As such, certain host traits may make certain individuals more susceptible to parasitism, which may affect observed patterns and costs of parasitism. For this thesis, I explored the patterns and consequences of parasitism using meta-analytical, experimental, and correlative approaches. Red squirrels (Tamiasciurus hudsonicus) were used to explore hypotheses in a wild host population. I found that several host traits affected patterns of parasitism. Group size scaled positively with parasite infection intensity and prevalence across a wide-breadth of vertebrate species in a meta-analysis, but only for parasites that were contact transmitted. Adult male red squirrels had higher flea infection intensities than females, but only when reproductively active and only as adults. Juveniles at birth had the highest flea intensities than at any other life-history stage. Nematodes had higher egg-shedding intensities in reproductively active hosts than in non-reproductive hosts, possibly owing to a trade-off between reproductive investment and immunity. The costs incurred by hosts appeared to be linked to the patterns of parasitism. For instance, through ectoparasite removal experiments, I found that parasitized juvenile red squirrels were lighter at emergence and less likely to survive from birth to emergence than their treated counterparts. Similarly, treated mothers spent significantly less time grooming than parasitized controls. The intensity of nematode egg shedding, but not flea intensity, was correlated with adult red squirrel body mass, suggesting a possible cost of endoparasitism to host condition. Finally, parasitism varied across i time, suggesting that the costs of parasitism may vary seasonally. My results indicate that parasites are distributed heterogeneously amongst their hosts, that parasites can alter the fitness and behaviour of their hosts, and that parasites, ultimately, have the potential to influence host life-histories and demography. ii Preface Contributions and Published Work Chapter 2 was previously published as Patterson, J. E. H., and K. E. Ruckstuhl. 2013. Parasite infection and host group size: a meta-analytical review. Parasitology, 140: 803-813. Copyright © 2013 J. E. H. Patterson and K. E. Ruckstuhl (Open Access). Reprinted with permission. JEHP developed the concepts and ideas, collected and analyzed the data, and wrote the manuscript; KER provided feedback and edited the manuscript. Chapter 3 contains a version of the unpublished manuscript by Patterson, J. E. H., P. Neuhaus, S. J. Kutz, and K. E. Ruckstuhl. Patterns of ectoparasitism in North American red squirrels (Tamiasciurus hudsonicus): sex-biases, temporal structure and effects on male body mass. JEHP designed the study, collected and analyzed the data, and wrote the manuscript. KER, PN, and SJK provided feedback and edited the manuscript. Chapter 4 was previously published as Patterson, J. E. H., P. Neuhaus, S. J. Kutz, and K. E. Ruckstuhl. 2013. Parasite removal improves reproductive success of female North American red squirrels (Tamiasciurus hudsonicus). PLoS ONE, 8(3): e55779. Copyright © 2013 J. E.H. Patterson, P. Neuhaus, S. J. Kutz, and K. E. Ruckstuhl (Open Access). Reprinted with permission. JEHP designed and performed the experiments, collected and analyzed the data, and wrote the manuscript; PN provided feedback and edited the manuscript; SK provided feedback; KER provided feedback and edited the manuscript. iii Ethics Statement The University of Calgary Life and Environmental Sciences Animal Care Committee (protocol #AC11-0088) approved the use of all animals and procedures employed in this study. All research and animal use complied with provincial and federal regulations. Permits for this work were obtained from the Fish and Wildlife Division of the Ministry of Environment and Sustainable Resource Development (Government of Alberta) and the Parks Division of the Ministry of Tourism, Parks and Recreation (Government of Alberta). iv Acknowledgements I would like to extend my gratitude to all of the people who helped make this research program possible. Most notably, my supervisor, K. Ruckstuhl, and unofficial co-supervisor, P. Neuhaus, who were constant sources of support, advice, encouragement, friendship, and inspiration throughout this entire process. My committee members, S. Kutz and R. Barclay, not only provided expert advice, lab space, supplies, and intelligent discussion, but also were instrumental in helping me formulate my ideas and keeping me focused. Although tasked with the under-appreciated role of having to examine me, I would like to extend a heartfelt thank you to L. Fedigan, R. Longair, M. Pavelka, and J. Waterman for serving on my candidacy and thesis defence committees. D. Whiteside helped with determining proper dosage for the anti-parasite medication and N. Parr assisted with fecal floatation training. I have made a lot of good friends through this journey who were always there to lend insight when I needed to talk, share a joke when I needed to laugh, or enjoy a beverage at the Grad Lounge when I was thirsty. Thanks to E. Baerwald, G. Beaudoin, B. Klug, L. Koren, L. May, K. Mosdossy, J. Reimer, J. Smith, and G. Uhrig. My lab mates in the Ruckstuhl lab provided a stimulating environment and many interesting discussions: D. Andres, C. Corbett, B. Edwards, B. Hoar, S. Liccioli, and P. McDougall. All of the researchers and staff at the R. B. Miller Kananaskis Field Station (most notably, J. Buchanan-Mappin, S. Dobson, A. Fahlman, M. Forrest, P. Neuhaus, A. Skibiel, and K. Yasuda) were always a great group of people to spend my field seasons with and were my family away from home. Of course, none of this would have been possible without the invaluable help from my very dedicated team of field and lab v assistants, to whom I am forever indebted: S. Majid, R. MacEachern, J. McMurray, and M. Zabrodski. It was a pleasure working with and learning from every single one of you! I gratefully acknowledge financial support from the Natural Sciences and Engineering Research Council of Canada (Canada Graduate Scholarship), Bettina Bahlsen Memorial and Queen Elizabeth II Scholarships, University of Calgary Thesis/Dissertation Grant, American Society of Mammalogists Grants-in-Aid of Research, and Alberta Conservation Association Grants in Biodiversity. Finally, I thank my family for their unrelenting love and support. vi To Oliver, for never ceasing to make me smile vii Table of Contents Abstract ................................................................................................................................ i Preface................................................................................................................................ iii Contributions and Published Work ................................................................................ iii Ethics Statement ............................................................................................................ iv Acknowledgements ..............................................................................................................v Table of Contents ............................................................................................................. viii List of Tables ..................................................................................................................... xi Epigraph ........................................................................................................................... xiii CHAPTER 1: INTRODUCTION ........................................................................................1 CHAPTER 2: PARASITE INFECTION AND HOST GROUP SIZE: A META- ANALYTICAL REVIEW ........................................................................................14 Introduction ....................................................................................................................14
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