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The Effect of Climate on Host-Parasite Interactions

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The Effect of Climate on Host-Parasite Interactions The Effect of Climate on Host-Parasite Interactions Emma Louise Gillingham A thesis submitted for the degree of Doctor of Philosophy (PhD) in the Organisms and Environment Division, Cardiff University June 2015 Declaration and Statements DECLARATION: This work has not been submitted in substance for any other degree or award at this or any other university or place of learning, nor is being submitted concurrently in candidature for any degree or other award. Signed.……………………………………………………………………………….. (candidate) Date ……………………… STATEMENT: This thesis is being submitted in partial fulfilment of the requirements for the degree of PhD Signed.……………………………………………………………………………….. (candidate) Date ……………………… STATEMENT: This thesis is the result of my own independent work/investigation, except where otherwise stated. Other sources are acknowledged by explicit references. The views expressed are my own. Signed.……………………………………………………………………………….. (candidate) Date ……………………… STATEMENT: I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loan and for the title and summary to be made available to outside organisations. Signed.……………………………………………………………………………….. (candidate) Date ……………………… STATEMENT: I hereby give consent for my thesis, if accepted, to be available for photocopying and for inter-library loans after expiry of a bar on access previously approved by the Academic Standards & Quality Committee. Signed………………………………………………………………………………… (candidate) Date……………………… i Acknowledgements First and foremost, I would like to thank my supervisors Sarah, Jo and Annapaola for giving me the opportunity to carry out this amazing project. You have all been wonderful mentors, and taught me so much. I especially want to thank Sarah for instigating my love of small mammals and their parasites, and going above and beyond the role of supervisor many times and being a wonderful friend (this doesn’t include the thunderstorm incident at Lake Garda). Your enthusiasm, friendship and support have meant the world to me, and I will really miss working with you. There are a number of people who have provided support to me. Jerzy Behnke (University of Nottingham) was a constant source of help when it came to parasite identification, and Michel Stanko, Stanislav Kaluz (Slovak Academy of Sciences), Eileen Harris and Rod Bray (NHM) also provided instrumental assistance. Jo Lello and Rob Thomas did the impossible and taught me statistics really could be fun; your patience and support was invaluable. I would also like to thank Valentina Tagliapietra for help with field site location in Trentino, and for being a great translator. Collecting all the data for this project would not have been possible without the hard work of many students. Luke, Emily, Marcos, Ben, Kieran, Kate and Jess helped me stay (relatively) sane in both the field and laboratory. I am incredibly grateful to FEM for funding this work, and the British Society for Parasitology for travel support to attend conferences to present and discuss my work in various locations. Thanks to my Italian amici who provided never-ending spritz, pizza, gelato and rugby: Fede, Ivana, Wibke, Michela, Irènè and Justin. I am particularly indebted to Maurizio and Luisa, for always being on hand to translate, teaching me all the Italian hand gestures, and never saying no to a gossip and a spritz. Thanks also extend to the Cardiff pub/coffee crew, but mostly my office mates through the years: Linda, Bettina, Alex, JoJ and Mike. I am especially grateful to El, Ellie, Fran and Jess, who kept me going, constantly encouraged coffee/cake/alcohol breaks and were/are always amazing. Thanks to Siân and Menna for forcing themselves to take a two-week holiday around Italy to make coming to Mezzocorona for the weekend worthwhile; you guys are the best. I absolutely could not have done this PhD without the support of my family. Mam, Dad, Helen and Graeme, thank you for your constant love and support, even though you thought my field seasons were really “holidays” and never really understood why I couldn’t just get a cat to catch mice for me. If only! Finally, Joe: my husband, co-driver and the best research assistant ever. Thank you for your never-ending support and love, no matter what country I was in. Our next adventure can now begin. “If there is one thing the history of evolution has taught us it's that life will not be contained. Life breaks free, it expands to new territories and crashes through barriers, painfully, maybe even dangerously, but…life finds a way” Ian Malcolm, Jurassic Park ii Thesis abstract Ecological systems are responding to changes in climate, and due to their ubiquitous nature, parasites will not be exempt from such changes. Understanding the effect that global climate change will have on parasites is of utmost importance, because there will be climate-driven implications for them and their hosts. This thesis addresses fundamental questions about the effect that a changing global climate will have on host- parasite interactions. First, a meta-analysis investigating general trends of parasites exposed to climatic perturbations found that warmer temperatures increased parasite abundance, did not affect fecundity and accelerated development time (Chapter 2). Field experiments were conducted in the Italian Alps, focussing on the yellow-necked mouse (Apodemus flavicollis) and its parasites as a model system. Low altitudinal sites (500 m) were significantly warmer and less humid than high altitudinal sites (1400 m), and as such, the change in altitude was used as a proxy for climate change. The effect of climate, host factors and parasite infection on one parasite life-history trait, in utero fecundity, was examined, and female hosts at low altitude harboured the least fecund parasites, which was posed to be driven by male-biased sex ratios in this cohort (Chapter 3). The effect of coinfecting parasites on the egg shedding-infection load relationship was further investigated, and this relationship was altered in coinfected hosts (Chapter 4). Interactions between coinfecting ectoparasites and helminths were quantified, and were found to be driven by host biology and climatic conditions (Chapter 5). Finally, infection with tick-borne endosymbionts and/or pathogens on tick behaviour was examined, and ticks infected with endosymbionts emigrated from dead hosts faster than uninfected individuals (Chapter 6). This thesis highlights the importance of considering the effect of host biology and coinfecting parasites in combination with climate when investigating the effect that future climatic changes may have on host-parasite interactions. iii Contents Declaration and Statements……………………………………………………... i Acknowledgements………………………………………………………………. ii Abstract…………………………………………………………………………... iii Contents…………………………………………………………………………... iv List of Figures……………………………………………………………………. vii List of Tables……………………………………………………………………... viii 1 General introduction: Climate change and host-parasite 1 interactions…............................................................................................... 1.1 Chapter overview……………………………………………………. 2 1.2 Climate change, ecological systems and their parasites…………….. 2 1.3 Host biology and parasitism…………………………………............ 8 1.4 The effect of coinfection on parasitism…………………….……….. 9 1.5 Investigating the effect of climate and host biology on host-parasite interactions in a free-living system………………………………….. 11 1.6 Thesis aims 11 2 The effect of temperature perturbations on parasite life-history 13 traits: a meta-analysis……………………………………………………. 2.1 Abstract……………………………………………………………… 14 2.2 Introduction………………………………………………………….. 14 2.3 Materials and methods………………………………………………. 17 2.3.1 Meta-data compilation………………………………...…….. 17 2.3.2 Meta-analysis…………………………………………...…… 18 2.4 Results……………………………………………………………….. 19 2.4.1 Parasite abundance………………………………………....... 21 2.4.2 Parasite fecundity……………………………………………. 22 2.4.3 Parasite development time…………………………………... 23 2.4.5 Host-parasite taxa and parasite abundance, fecundity and 24 development time……………………………………….....… 2.5 Discussion…………………………………………………………… 26 2.6 Author acknowledgement…………………………………………… 29 iv 3 The effect of climate, host and parasite factors on parasite fecundity... 30 3.1 Abstract……………………………………………………………… 31 3.2 Introduction………………………………………………………….. 31 3.3 Materials and methods………………………………………….…… 34 3.3.1 Field sampling……………………………………………….. 34 3.3.2 Quantifying nematode abundance and fecundity……………. 35 3.3.3 Climate data…………………………………………………. 36 3.3.4 Statistical analysis…………………………………………… 37 3.4 Results……………………………………………………………….. 37 3.5 Discussion…………………………………………………………… 42 3.6 Author acknowledgement…………………………………………… 44 4 Are the most infected hosts also the most infectious? The relationship 45 between parasite burden and egg shedding in coinfected hosts……….. 4.1 Abstract……………………………………………………………… 46 4.2 Introduction………………………………………………………….. 46 4.3 Materials and methods………………………………………………. 48 4.3.1 Field sampling……………………………………………….. 48 4.3.2 Statistical analysis…………………………………………… 49 4.4 Results……………………………………………………………….. 50 4.4.1 Heligmosomoides polygyrus intensity-infectiousness 51 relationship…………………………………………………... 4.4.2 Rodentolepis straminea intensity-infectiousness 52 relationship…………………………………………………... 4.4.3 Diversity of helminths in the gastrointestinal tract verses the 53 faeces………………………………………………………... 4.5 Discussion…………………………………………………………… 53 4.6 Author acknowledgement…………………………………………… 57 5 Interactions
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