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Macroparasites of the Eurasian Otter: Distribution, Life-Cycles and Population Dynamics

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Macroparasites of the Eurasian Otter: Distribution, Life-Cycles and Population Dynamics Macroparasites of the Eurasian Otter: distribution, life-cycles and population dynamics A thesis submitted to Cardiff University for the degree of Doctor of Philosophy by Ellie Sherrard-Smith, BSc. (Hons) ACKNOWLEDGEMENTS APPENDIX 1: Specimen layout for Thesis Summary and Declaration/Statements page to be included in a Thesis 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 ……10 July 2013…… STATEMENT 1 This thesis is being submitted in partial fulfillment of the requirements for the degree of PhD. Signed ……………… ……… (candidate) Date …10 July 2013……… STATEMENT 2 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 ……10 July 2013…… STATEMENT 3 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 …10 July 2013……… STATEMENT 4: PREVIOUSLY APPROVED BAR ON ACCESS 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 …10 July 2013…… ACKNOWLEDGEMENTS ACKNOWLEDGEMENTS Contributions to data A large proportion of the samples for this PhD were collected at post mortem by members of the Cardiff University Otter Project. Thanks to all those who contributed through performing post mortems and archiving samples and records. Thank you especially to Dr Liz Chadwick for allowing me to use the samples for this thesis. I was fortunate to have some good students during my PhD time. Aaron Nahil worked on the ticks collected from otters and contributed to identifying approximately half of those used in this PhD (chapter 3). Matt Wyman processed some of the gall bladders (200 out of 586) for his dissertation and these data (presence/absence, intensity and fibre score) were included in this PhD. Thank you to Chris Williams and Amy Reading from the Environment Agency for providing metacercariae samples and all prevalence data on fish cysts for the life cycle chapter (chapter 7). Thank you to Dr Andrew Conlan (Cambridge University) for advising and teaching me about modelling (Chapter 8). My Supervisors I can not thank Liz and Jo enough for the constant support, advice, guidance and friendship they have provided over the past few years. It has been a pleasure to work with and alongside both. Even when away on maternity Liz has made herself available to read through drafts or chat through ideas. Jo has pushed me to work harder and understand better all aspects of research whilst maintaining a passion for the subject. Both are outstanding supervisors. Thank you both! My friends and family The Cardiff University Research into Infection Parasitology and Ecology Society (CRIPES) was instrumental in my development over the time I have spent at Cardiff. I was incredibly fortunate to work alongside Sarah Perkins whose enthusiasm and support has been sensational and who was particularly brilliant during the write up of chapter 6. Thank you to Perky for cycling to France with me for samples – a fun and windy trip!! Also Jo Lello was an excellent friend to turn to for support and advice especially whilst writing up chapter 8. Thank you to Pablo – legend. I cannot put into words how fun and supportive Eleanor Kean, Suz Williams, Emma (Roidy) Gillingham, Jess Stevenson and Fran Hockley have been during my time at Cardiff. You are all sensational. Thank you to the revolution (Drs Eleanor Kean, TC and J Randall). Tom Crowther was epic whenever we had breaks and at times a true friend. His and Steve’s (Thomas) distractions will have prepared me to work in any climate from now on! James Vafidis has made the final year brilliant. Everyone in the 5th, 6th and 7th floors during my time in BIOSI 2 were splendid. My football team Cardiff for the ideal distraction and letting me off when the PhD distracted me… My friends outside uni were always brilliant, a shoulder and company whenever I needed help. Especially Hanna banana who came along on snail collecting trips! My family were equally brilliant and I love you all! Thank you especially to Twiglet who has taken the brunt of the tougher times toward the end! ACKNOWLEDGEMENTS TABLE OF CONTENTS TABLE OF CONTENTS Summary…………………………………………………………….. vii List of Tables ………………………………………………………... viii List of Figures……………………………………………………….. xi Chapter 1. A General Introduction 1 1.1 Parasites: A global issue…………………………………… 1 1.2 Parasite Distributions………………………………………. 1 1.3 Abiotic and Biotic Associations …………………………… 3 1.4 Thesis aims…………………………………………………. 3 1.5 References……..…………………………………………… 5 Chapter 2 8 Literature Review: How do abiotic and biotic factors determine the host-parasite distribution patterns observed in trematode populations of mammalian hosts? 2.1 Abstract……………………………………………………. 8 2.2 The importance of parasites……………………………… 8 2.3 Abiotic interactions……………………………………….. 9 2.3.1 Meteorological conditions……………………………….. 9 2.3.2 Season and annual patterns………………………………. 15 2.3.3 Land use and habitat ecology…………………………….. 15 2.3.4 Anthropogenic impacts…………………………………... 16 2.4 Biotic interactions.………………………………………... 18 2.4.1 Diet………………………………………………………. 18 2.4.2 Host sex and age…………………………………………. 18 2.4.3 Parasite competition and co-infection……………………. 23 2.4.4 Trematodes as generalists………………………………... 25 2.5 Combined impacts of abiotic and biotic factors………… 25 2.6 Conclusions and future directions……………………….. 26 2.7 References..………………………………………………… 27 Chapter 3 38 Abiotic and biotic factors associated with tick population dynamics on a mammalian host: Ixodes hexagonus infesting otters, Lutra lutra 3.1 Abstract……………………………………………………. 38 3.2 Introduction……………………………………………….. 39 3.3 Materials and Methods…………………………………… 40 iii TABLE OF CONTENTS 3.3.1 The host………………………………………………….. 40 3.3.2 Parasite identification……………………………………. 41 3.3.3 Data preparation………………………………………….. 42 3.3.4 Data analysis……………………………………………... 43 3.4 Results……………………………………………………... 45 3.4.1 Tick species………………………………………………. 45 3.4.2 Abiotic factors……………………………………………. 45 3.4.3 Biotic factors……………………………………………... 48 3.5 Discussion………………………………………………….. 48 3.6 Acknowledgements………………………………………... 53 3.7 References..………………………………………………… 53 Chapter 4 58 Climate variables are associated with the presence of biliary trematodes in otters 4.1 Abstract……………………………………………………. 58 4.2 Introduction……………………………………………….. 58 4.3 Materials and Methods…………………………………… 61 4.3.1 Sample preparation………………………………………. 61 4.3.2 Species identification…………………………………….. 61 4.3.3 Gall bladder damage………...…………………………… 62 4.3.4 Spatial and temporal trends………………………………. 62 4.3.5 Abiotic Associations……….………………………….… 63 4.4 Results……………………………………………………... 65 4.4.1 Spatial and temporal geographic trends…………………. 65 4.4.2 Biotic Associations………………………………..……... 66 4.4.3 Abiotic Associations…………………………………….. 68 4.5 Discussion…………………………………………………. 69 4.6 Acknowledgements……………………………………….. 75 4.7 References………..………………………………………… 75 Chapter 5 83 Distribution and molecular phylogeny of biliary trematodes (Opisthorchiida) infecting fish-eating mammals (Lutra lutra and Mustela vison) across Europe 5.1 Abstract……………………………………………………. 83 5.2 Introduction……………………………………………….. 84 5.3 Materials and Methods…………………………………… 87 5.3.1 Sample collection………………………………………… 87 5.3.2 DNA analysis…………………………………………….. 88 5.4 Results……………………………………………………... 89 iv TABLE OF CONTENTS 5.5 Discussion………………………………………………….. 94 5.6 Acknowledgements………………………………………... 96 5.7 References……..…………………………………………… 96 Appendix 5.1………………………………………………….. 102 Chapter 6 108 Spatial and seasonal factors are key determinants in the aggregation of helminth populations in their definitive hosts: Pseudamphistomum truncatum in otters Lutra lutra 6.1 Abstract……………………………………………………. 108 6.2 Introduction……………………………………………….. 109 6.3 Materials and Methods…………………………………… 111 6.3.1 Sample collection………………………………………… 111 6.3.2 Aggregation parameters………………………………….. 112 6.3.2.1 The corrected moment estimate k……………….. 113 6.3.2.2 Taylor’s Power Law……………………………... 113 6.3.2.3 The Index of Discrepancy (D)…………………… 114 6.3.2.4 Boulinier’s ‘J’……………………………………. 115 6.3.3 Parasite fecundity………………………………………… 116 6.4 Results……………………………………………………... 117 6.4.1 Parasite abundance………………………………………. 117 6.4.2 Parasite aggregation……………………………………… 117 6.4.3 Parasite fecundity………………………………………… 122 6.5 Discussion………………………………………………….. 123 6.6 Acknowledgements………………………………………... 127 6.7 References..………………………………………………… 127 Chapter 7 132 New intermediate hosts identified for two trematodes established in otter (Lutra lutra) populations in the UK 7.1 Abstract……………………………………………………. 132 7.2 Introduction……………………………………………….. 133 7.3 Materials and Methods…………………………………… 134 7.3.1 The first intermediate host……………………………….. 134 7.3.2 The second intermediate hosts…………………………… 136 7.3.3 Molecular identification of larvae………………………... 137 7.3.4 Alternative definitive host………………………………... 138 7.4 Results……………………………………………………... 138 7.4.1 The first intermediate hosts: gastropods…………………. 138 7.4.2 The second intermediate hosts: cyprinid fish…………….
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