THE UNIVERSITY OF HULL Ecological implications of introducing Leucaspius delineatus (Heckel, 1843) and Pseudorasbora parva (Temminck and Schlegel, 1842) into inland waters in England Being a Thesis submitted for the Degree of Doctor of Philosophy at the University of Hull, United Kingdom by Kathleen Beyer M.Sc. (Aquatic Tropical Ecology), University of Bremen, Germany, 2002 May 2008 i In Gedenken an meinen wundervollen Opa, der nie aufgehoert hat, sich Wissen anzueignen und von dem ich sehr viel gelernt habe. Kurt Kramer Du kannst Tränen vergießen, weil er gegangen ist. Oder Du kannst lächeln, weil er gelebt hat. Du kannst die Augen schließen und Beten, dass er wiederkehrt. Oder Du kannst die Augen öffnen und all das sehen, was er hinterlassen hat. (VerfasserIn unbekannt) ii Widmung Diese Doktorarbeit widme ich meinen Eltern, Hannelore und Reinhard Beyer, für ihre stete Unterstuetzung in allen Lebenslagen. Dedication I dedicate this doctoral dissertation to my parents, Hannelore and Reinhard Beyer, for their constant support in all my endeavours. iii ‘’All animals are equal, but some animals are more equal than others.’’ George Orwell, Animal Farm, 1951 iv Acknowledgements A large number of people have crossed my way throughout the PhD and have encouraged and inspired me. They all helped with the success of this work in one way or the other. It is impossible to mention everyone here, but I am indebted to you all! With much gratitude I thank Dr Rodolphe Gozlan (Rudy), my day-to-day supervisor, whose enthusiasm and relentless support gave me much motivation every single day. With much appreciation, I would like to thank my supervisor Dr Gordon Copp for his tireless support and advice throughout my PhD. Thank you for always being there to help, for answering my questions and for correcting my English. Many thanks to Professor Ian Cowx for his much appreciated advice and valuable recommendations throughout. Thank you to Dr Steve Feist and Dr Matt Longshaw for their support with anything regarding parasites. Thank you to all for your efforts in securing funding for this project, for sharing your knowledge with me and for accepting me as a scientist. Thank you to all of you for meticulously reading through the numerous thesis drafts and for your advice on their improvement. I hope we can work together in the future. A big thank you goes to the Fish Ecology Group at the Centre for Ecology and Hydrology in Dorset. Thank you to Adrian Pinder, Dr Anton Ibbotson, Bill Beaumont, Luke Scott and Rudy for welcoming me in the ‘Fish Team’. I couldn’t have done this without your support! Thank you to the many people who were indispensable in the field and the laboratory. These people played a great part in the success of this project: Alexander Lawrence, Angel Ferrero Serrano, Brenda Asmus, Dörte Beyer, Francois Dubusse, James Coombes, Jennifer Nightingale, Julie Monroux, Lisa Allen, Sarah Warriss and Saulius Stakenas. Particular gratitude goes to Alastair Cook for his invaluable help with much of the field work. Many thanks go to Judith Wardlaw for her support and the coordination of students at CEH Dorset. Many thanks to Jon Bass for help and advice on invertebrate identification. Thank you to Danuta Kochanowska for guidance on parasitological investigations in fish. Many thanks to Adrian Pinder for his advice on larval fish identification. Thank you also to Dr Rafael Miranda, for inspiring a new idea for a new manuscript that has become a publication. Thank you to the anonymous referees who gave advice on how to improve manuscripts that have now been published. Thank you to Dr Michael G. Fox for supplying the Excel macro for the life history calculations. Thank you to Steve Borgatti and Malcolm Baptie for their advice in the use of UCINET and social network analysis. Thanks to the numerous fishery-, land- and water-owners who granted me access to the various field sites. The staff of the Environment Agency were invaluable for their rapid response to grant me the necessary fishing licences and advising on site access. Thank you to the Eastleigh District Angling Club, Revels Fishery, specifically to Paul Martin, Robin and Maureen Lawres and Mark Stollery for being so helpful and for granting me access to ‘my’ fisheries at odd times. Thanks to all the friends that have been there one way or the other, I couldn’t have done it without you! Thank you to Alison Poole, Beth Mott, Bob Muscarella, Carmen Feil, Demetra Andreou, Helen Palmer, Helen Vincent, v Jennifer Selgrath, Jill Ashton, Johnny Stornante, Jon Stacey, Judith Ambros, Mike Bowes, Morag McCracken, Nicola Gammans, Wendy Knerr, and Zoe Randle. Special thanks go to Dörte Beyer and Tim Lüdrichsen for their support, and to Jude for the many years of friendship. I am indebted to Morag and Mike, who gave me a home during the final and crucial stages of completion of this PhD thesis. Thanks also to their dog Meg for keeping me company during this time. Thanks to the ‘Horns of Plenty’ for the music. My deepest appreciation goes to my family, particularly to my parents, Hannelore and Reinhard Beyer, for their relentless support throughout all my endeavours. Thank you to my sister, Dörte, for always being there for me. Thank you to all my family for believing in me and for enabling me to choose my way in life. I am grateful to the U.K. Department of Food and Rural Affairs (Defra) for their sponsorship. Thank you to the Centre for Ecology and Hydrology in Dorset for hosting me, and a special thank you to all the staff that have assisted me over the years. Finally I would like to thank Dr Rob Britton and Dr Jon Harvey, my PhD examiners, for their time and the advice they have provided to improve this final document. vi Abstract Non-native species invasions threaten the structure, function and biodiversity of ecosystems worldwide, and those of non-native fishes pose amongst the greatest threats to inland waters of the U.K. This PhD investigated the establishment, dispersal and ecological implications of introducing the two non-native fish species, sunbleak Leucaspius delineatus (Heckel, 1843) and topmouth gudgeon Pseudorasbora parva (Temminck and Schlegel, 1842) to inland waters of England. The introduction and initial dispersal of both species can be attributed to the commercial fish trade. Species-specific variability of life history, growth and morphological traits was examined in sunbleak (12 sites) and topmouth gudgeon (3 sites) to assess their role in establishment success. The drift dynamics, i.e. timing and intensity (propagule pressure), of sunbleak and topmouth gudgeon were assessed for source populations to determine dispersal potential. Potential risks for native species posed by these two alien cyprinids were assessed with respect to the parasite fauna and overlaps in resource use. For sunbleak, these were also examined in terms of social integration of this species into a native fish assemblage. Biological resistance to topmouth gudgeon invasion was evaluated by stomach flushing and gut content analysis of native piscivorous fishes. Inter-population variability in life histories and morphological characters were observed in both sunbleak and topmouth gudgeon. Populations of both species matured at small body sizes and between the ages 1 and 2. The fish were of good body condition and exhibited high reproductive investment. In both species, dispersal from source waters followed a diel pattern, with higher rates at night than during the day (e.g. maximum drift densities during May of 2004 and 2005: 9-10 sunbleak per 1000 m-3 at about 23:00 hrs; 40-52 topmouth gudgeon per 1000 m-3 at about 05:00 hrs). Downstream of one source population, microhabitat use of topmouth gudgeon was found to overlap with native species (brown trout Salmo trutta L., European chub Leuciscus cephalus (L.), bullhead Cottus gobio L., stoneloach Barbatula barbatula (L.); both brown trout and chub were observed to prey on topmouth gudgeon. However, predation intensity may be density-dependent and of insufficient level to impede topmouth gudgeon establishment, which was facilitated in the receiving stream by the consistent propagule pressure from on-line source populations. Sunbleak diet and microhabitat use also overlapped with native species (roach Rutilus rutilus (L.) and common bream Abramis brama (L.)) as young larvae, but this decreased with age. Social network analysis of sunbleak-native species interactions revealed that sunbleak creates significantly stronger social bonds with the native species than do natives amongst themselves. No macro-parasites were found in topmouth gudgeon, but two ‘Category II’ non-native parasites Neoergasilus japonicus (Harada, 1930) and Ergasilus briani (Markewitsch, 1932) were found in some populations of sunbleak. The potential for sunbleak to spread beyond their current distribution in England and the species’ social integration behaviour may facilitate the dispersal of these parasites, which may spread faster among communities invaded by sunbleak than in those where this non-native species is absent. The results of this PhD study are discussed within their wider context and their relevance to non-native species risk analysis and management. vii Table of Contents Acknowledgements ............................................................................................. v Abstract ............................................................................................................. vii Table of Contents ............................................................................................