The impact of invasive crayfish on aquatic ecosystems A thesis submitted for the degree of Doctor of Philosophy (Ph.D) by Joanna James November 2015 School of Biosciences Cardiff University i Declaration and Statements 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 24.11.15…………………….. STATEMENT 1 This thesis is being submitted in partial fulfilment of the requirements for the degree of PhD. Signed …………………………………… (candidate) Date 24.11.15………………………… 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 24.11.15………………………… 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 24.11.15 ………………………… 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 24.11.15………………………… ii Acknowledgments ACKNOWLEDGMENTS So many people to thank, where do I begin! Thank you so much to my primary supervisor and great friend, Prof. Jo Cable for all her academic and emotional support throughout the last four years. There have been times I have turned up at your office in despair and half an hour and a coffee later you have fixed everything! Thanks also to my co-supervisor, Dr Ian Vaughan for always being calm and reassuring and providing statistical support! Dr Fred Slater, thank-you for introducing me to my first crayfish and for being a font of knowledge and the best conference companion anyone could hope for. Thanks to my external supervisors at Natural Resources Wales, Dr Kyle Young and Catrin Grimstead. Kyle, thank you for all your support, particularly on the meta-analysis. Catrin, thank you for helping me with the compilation of CrayBase and for keeping me in touch with the “real world” outside of academia. Thanks to both my collaborators who have supported my research visits to their labs; Drs Adam Petrusek and Andy Mackie, I learned so much from you both. Thanks also to Agata M, Adam Ellis, Birgit O, Alberto M, David Holdich and Stephanie Peay for being excellent collaborators and helping me to expand my horizons. I am also extremely grateful to Prof. Maurice Rolls and his wife Jane for their kindness, for allowing me to conduct field surveys near their home and affording me the opportunity to participate very enjoyable community awareness events. Thanks to all my office mates and BioSci buddies: Bettina, Em, Fran, Jess, Mike, Willow, Alex, Kate D, Rhian N, Marian Pye (and everyone else on the 6th floor), Catrin W, Elle SS, in particular Linda, Rhids and Graham. Also thanks to the army of students who I supervised during my PhD; Rhidian Thomas, Kate Davidson, Graham Richardson, Clare Baranowski, Robby Mitchell, Kate Worsley-Tonks, Kamila Mustafina, Vane L and Jordan Fox. To my long suffering family and friends: thanks to my parents and brother, Jon, for being supportive, if not entirely understanding, of my decision to study crayfish! Thanks to my mother-in-law, Angela Ellis, for being so supportive. Thanks to my very best friend, Claire Bissett for coming out on fieldwork adventures with me and generally always being there for me. Thanks also to Rob and Mary Bissett, who have been like second parents to me throughout this whole process. Finally thanks to my boyfriend, and willing fieldwork assistant, Nathan Iliescu. Thank you so much for giving up your summer to help me survey crayfish and for being extremely supportive throughout my PhD; all you have done means so much to me. Thank you all iii Contents CONTENTS TABLE OF CONTENTS DECLARATION AND STATEMENTS ................................................................................ ii ACKNOWLEDGEMENTS .................................................................................................... iii CONTENTS ............................................................................................................................. iv TABLE OF CONTENTS .......................................................................................................... iv LIST OF FIGURES ................................................................................................................. viii LIST OF TABLES .................................................................................................................... xi SUMMARY ............................................................................................................................... x CHAPTER 1: GENERAL INTRODUCTION ...................................................................... 1 1.1 Overview .................................................................................................................. 2 1.2 The ecological impacts of crayfish on other aquatic organisms and ecosystem processes ........................................................................................................................ 3 1.3 Crayfish as invasive species ..................................................................................... 6 1.3.1 Global spread and invasiveness ................................................................. 6 1.3.2 Interactions with native crayfish................................................................ 7 1.4 Factors influencing non-native crayfish invasion dynamics ................................... 8 1.4.1 Interspecific interactions between non-native crayfishes .......................... 8 1.4.2 Host-parasite interactions .......................................................................... 9 1.4.2.1 Aphanomyces astaci, the causative agent of crayfish plague ..... 9 1.4.2.2 Ectosymbiotic branchiobdellidans (Annelida: Clitellata)......... 10 1.5 Thesis aims ............................................................................................................. 11 1.6 Thesis layout ........................................................................................................... 11 1.7 References .............................................................................................................. 12 CHAPTER 2: Comparing the ecological impacts of native and invasive crayfish: could native species’ translocation do more harm than good? ..................................................... 20 2.1 Abstract ................................................................................................................... 21 2.2 Introduction ............................................................................................................ 22 2.3 Methods .................................................................................................................. 23 2.3.1 Study selection and data extraction ......................................................... 23 2.3.2 Effect size calculations ............................................................................ 25 2.3.3 Statistical analysis ................................................................................... 25 2.4 Results .................................................................................................................... 26 2.5 Discussion ............................................................................................................... 28 2.5.1 Conclusions and management implications ............................................ 31 2.6 References .............................................................................................................. 32 iv Contents CHAPTER 3: A.L.I.E.N. databases: Addressing the Lack In Establishment of Non- natives databases .................................................................................................................... 36 3.1 Abstract ................................................................................................................... 37 3.2 Introduction ............................................................................................................ 38 3.3 Methods .................................................................................................................. 39 3.4 Results .................................................................................................................... 39 3.5 Discussion ............................................................................................................... 41 3.6 References .............................................................................................................. 43 CHAPTER 4: Over-invasion in a freshwater ecosystem: newly introduced virile crayfish outcompete established invasive signal crayfish .................................................................. 45 4.1 Abstract ................................................................................................................... 46 4.2 Introduction ...........................................................................................................