Why are invaders invasive? Development of tools to understand the success and impact of invasive species Nigel Gareth Taylor Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds School of Biology September 2016 ii The candidate confirms that the work submitted is his own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given within the thesis where reference has been made to the work of others. Chapter Three is based on a jointly authored publication: Taylor, N.G. & Dunn, A.M. (2016) Size matters: predation of fish eggs and larvae by native and invasive amphipods. Biological Invasions. DOI: 10.1007/s10530-016-1265-4 Nigel Taylor developed the idea, conducted the experiments, analysed the data and wrote the manuscript. Alison Dunn formulated the idea, supervised the research and contributed to writing the manuscript. Caroline Liddell provided assistance in conducting the experiments. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. © 2016 The University of Leeds and Nigel Taylor The right of Nigel Taylor to be identified as Author of this work has been asserted by him in accordance with the Copyright, Designs and Patents Act 1988. iii iv Acknowledgements Sincere thanks go to my supervisor, Alison Dunn. You have offered continued guidance and support when needed, on intellectually stimulating topics as well as mundane logistical ones, but also allowed me freedom to make my own mistakes. I also thank other researchers at Leeds for continued general support and feedback, especially Sarah Zylinski, Christopher Hassall, Keith Hamer, Melanie Hatcher, Anita Glover and Rupert Quinnell. I thank my undergraduate tutor, Graham Taylor for helping me to think critically about biology. I am extremely grateful for a scholarship from the Natural Environment Research Council which funded the majority of this research, with additional contributions from water@leeds. I thank Tanya Ferry (Port of London Authority), the Environment Agency and Leeds City Council for granting access to collect animals from their waterways. Thanks to my fellow PhD students at the University of Leeds: Paula Rosewarne, Katherine Arundell, Asa Johannesen, Stephanie Peay, Mandy Bunke and Lucy Anderson for showing me many ropes and putting up with my naiveté in the initial phases of my PhD. Tom Doherty-Bone, Jamie Bojko, William Fincham, Caitriona Shannon, Daniel Warren and Giovanna Villalobos- Jimenez continue to offer thoughtful discussion and reassuring conversation. Finally, I am hugely grateful for the support of my friends and family. Mum and Dad, your unwavering support has given me a solid foundation and the confidence to complete this PhD. Alex and Charlotte, your pragmatism has kept me grounded (and the crab-hunting accommodation was much appreciated). Gloria and Gael, thanks for making me feel at home in Leeds. v Specific acknowledgements by Chapter: Chapter 2: Rachel Paterson advised on experimental analysis. Paula Rosewarne assisted with counting chironomid larvae. Chapter 3: Epperstone Park Hatcheries and Northern Trout (Brow Well Fisheries Ltd.) for supplied fish eggs and Calverton Fish Farm advised on sourcing. Angela Tarry and Anglian Water allowed access to Grafham Water collect amphipods. Caroline Liddell assisted with laboratory work using trout eggs and larvae. David Aldridge, Chris Hassall, Calum MacNeil, and Rachel Paterson advised on animal collection, experimental design and analysis. Two anonymous reviewers, and the Dunn and Hassall Lab Groups, provided insightful comments on drafts of the Chapter. Chapter 5: Additional funding for this work was secured through a water@leeds SPRING grant. Numerous angling clubs and their members allowed access to their waters, including Phil Bamforth (Yorkshire Anglers), David Griffiths (Tanfield Angling Club), Brian Morland (Bellflask Fishery), Mr M Thompson (Long Preston Beck) and Mr P Fawcett (Bookill Gill Beck). Stephanie Peay and Gareth Jones advised on crayfish distributions. Lee Brown, Graham Askew and Tom Doherty-Bone advised on, and/or provided equipment for, respirometry. Danielle Lawton assisted with animal husbandry. Chapter 6: Melanie Hatcher contributed to idea development and provided feedback on drafts of the chapter. Andrew West assisted with protist culture methods and bacteriology. Danielle Lawton and Alex Simpson provided patient assistance and input during the initial stages of working with the microcosm systems. vi Abstract Biological invasions are a major facet of anthropogenic global change, with severe negative environmental and socioecological impacts. Effective and efficient management of biological invasions requires a mechanistic understanding of the factors driving invasion success and impact. I investigate three factors likely to have broad relevance in explaining success and impact of alien invaders: resource use, behaviour and propagule pressure. Alien decapod and amphipod crustaceans may have different patterns of trophic resource use to native analogues. Through quantification of functional responses and food ‘choice’, I highlight an exceptionally large predatory impact of alien Eriocheir sinensis on invertebrate prey, relative to both native and alien crayfish. Through similar methods, I suggest the larger size of alien Dikerogammarus villosus relative to native Gammarus pulex could facilitate higher predatory impacts on fish eggs and larvae. I quantify personality traits (boldness, exploration, activity, sociability and voracity) of invasive and native decapod crustaceans in the laboratory. Invasive E. sinensis and Pacifastacus leniusculus were bolder than European Austropotamobius pallipes. Boldness may a common trait of successful, high-impact invaders. I provide the first evidence of personality (consistent within- individual behaviours) in these decapods, but find no evidence that it drives dispersal in signal crayfish. Comparisons of core and invasion-front populations of P. leniusculus suggest its spread is driven by density rather than behaviour. Using experimental invasions of ciliate protists into laboratory microcosms, I provide quantitative data to show how propagule pressure – the number of introduced organisms and introduction events – can increase invasion success (rate and population density) and invader impact. In general, resource use, behaviour and propagule pressure all have potential to predict the identity, impact and dynamics of successful invaders and thus inform management strategies. Having measured metabolism alongside these other factors, I propose that metabolic rate could provide another readily-measurable, general predictor of invasion success and impact. vii List of Abbreviations AAS Absolute aerobic scope AIC Akaike’s information criterion ANOVA Analysis of variance CE Common Era cmax Maximum carapace dimension CPUE Catch per unit effort df Degrees of freedom DO Dissolved oxygen FR Functional response GLM Generalised linear model LM Linear model MAM Minimum adequate model ṀO2 Rate of oxygen consumption MMR Maximum metabolic rate MR Metabolic rate NNSS Non-Native Species Secretariat PCA Principal component analysis PVC Polyvinyl chloride RMR Routine metabolic rate SE Standard error SMR Standard metabolic rate viii Table of Contents Abstract .......................................................................................................................... vii List of Abbreviations .................................................................................................... viii List of Figures................................................................................................................ xiii List of Tables .................................................................................................................. xv Chapter 1 Introduction: the problem of biological invasions ...................................... 1 1.1. Outline................................................................................................................................ 1 1.2. The Anthropocene and biological invasions ...................................................................... 1 1.2.1 Terminology and the invasion process ......................................................................... 2 1.2.2 Why are biological invasions important? ..................................................................... 5 1.3 Management of biological invasions .................................................................................. 7 1.3.1 Management through the invasion process .................................................................. 7 1.3.2 What to manage: risk assessment ................................................................................. 8 1.3.3 How to manage: designing effective strategies .......................................................... 10 1.4. Mechanisms underlying invasion success and impact ..................................................... 10 1.4.1 Propagule pressure ..................................................................................................... 15 1.4.2 Behaviour ..................................................................................................................