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The Impact of Ponto Caspian Invaders on the Parasite Communities of Multiple Hosts Within West and Central European River Systems

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The Impact of Ponto Caspian Invaders on the Parasite Communities of Multiple Hosts Within West and Central European River Systems The impact of Ponto Caspian invaders on the parasite communities of multiple hosts within West and Central European river systems Dissertation zur Erlangung des Doktorgrades Dr. rer. nat. der Fakultät für Biologie an der Universität Duisburg-Essen vorgelegt von Michael Andreas Alfred Hohenadler geboren in Troisdorf 3.10.2018 I am a firm believer, that without speculation there is no good and original observation. Charles Darwin Angaben zur Prüfung Die der vorliegenden Arbeit zugrundeliegenden Experimente wurden in der Abteilung für Aquatische Ökologie der Universität Duisburg-Essen durchgeführt. 1. Gutachter: Prof. Dr. Bernd Sures 2. Gutachter: PD Dr. Franz Jirsa 3. Gutachter: Vorsitzender des Prüfungsausschusses: Prof. Dr. Florian Leese Tag der mündlichen Prüfung: 20.12.2018 Diese Dissertation wird über DuEPublico, dem Dokumenten- und Publikationsserver der Universität Duisburg-Essen, zur Verfügung gestellt und liegt auch als Print-Version vor. DOI: 10.17185/duepublico/47799 URN: urn:nbn:de:hbz:464-20191209-125038-9 Alle Rechte vorbehalten. Acknowledgements Foremost, I would like to express my sincere thanks to my advisor Bernd Sures for providing me with the opportunity to complete my PhD thesis at the University of Duisburg Essen, thanks for your continuous support, patience, motivation, immense knowledge, as well as for the many inspiring and humorous conversations. I could not have imagined a better mentor for my PhD study. Special thanks to Franz Jirsa who shared his knowledge, lab and house with me. Furthermore, I want to pronounce my gratitude to Milen Nachev who was very dedicated to his role as my secondary supervisor. Thanks for being there for me to exchange ideas and for the numerous motivating discussions. Thanks to Daniel Grabner for sharing your knowledge about molecular biology (and many other things) with me. My sincere thanks also goes to all co-authors that are part of the published articles, for your support, contributions and help. I also want to thank my current and former fellow PhD students and co-workers. Thanks to Christian Selbach, Michelle Pahl, and Marion Woermann for umpteen entertaining hours and thoughtful conversations – you are simply the best and funniest office mates I can think of. Thanks to Katrin Honka, Thomas Meissner, and Jan Lemm for motivating me to leave work and to do sports instead – at least sometimes you were successful. Thanks to Jessica Schwelm for the many walking tours and deep conversations. Thanks to Jan Lemm and Louisa Rothe for your help with the graphic realization of some of my ideas. Thanks to Julian Enss, Katrin Honka, Diana Michler, and Jenia Kremers for directly supporting me by gathering and/or examining my samples. Thanks to Benjamin Kupilas, Caroline Winking, Maria Ceylan, Jessica Schwelm, Alexander Gieswein, Christian Feld, Mark Schumann, Henrike Hamer, Martin Sondermann, Maria Gies, Sonja Zimmermann, Thomas Knura, Birgit Rieth, Nina Kaiser, Daniel Hering, Kerstin Dangel, Armin Lorenz, everyone I mentioned before, and the rest of the Aquatic Ecology department for encouraging me in one or another way. I would also express special thanks to the Deutsche Bundesstiftung Umwelt (DBU) and Volker Wachendörfer that made this work possible. Furthermore, I acknowledge funding by the Faculty of Biology at the University of Duisburg-Essen as well as travel grants by the German Academic Exchange Service (DAAD). Finally, but by no means least, thanks to David John Yabis for your constant support, and believe in me, thanks for always being there for me. Thanks to Elke Hohenadler Manuela Hohenadler, Louise Jagemann, and Hans Hohenadler (I know you were always with me), and to all my friends for your love, believe, and support. Dear family, I dedicate this thesis to all of you Table of contents List of abbreviations………………………………………………………………….. 8 List of figures………………………………………………………………………….. 9 List of tables…………………………………………………………………………... 11 1 Summaries………………………………………………………………………….. 13 1.1 Summary………………………………………………………………….. 13 1.2 Zusammenfassung.……………………………………………………… 15 2 General introduction.………………………………………………………………. 18 2.1 Background……………………………………………………………….. 18 2.2 Aims and hypotheses……………………………………………………. 23 3 General material and methods……………………………………………………. 25 3.1 Study area………………………………………………………………… 25 3.2 Sampling…………………………………………………………………... 27 3.3 Parasitological analysis………………………………………………….. 30 Chapter I: Direct effects of Ponto-Caspian invasion on local fish parasite communities by the example of three native and one invasive host species….. 35 4 How Ponto-Caspian invaders affect local parasite communities of native fish……………………………………………………………………………………… 36 4.1 Summary………………………………………………………………………….. 36 4.2 Introduction……………………………………………………………………….. 37 4.3 Material and methods……………………………………………………………. 40 4.4 Results…………………………………………………………………………….. 45 4.5 Discussion………………………………………………………………………… 58 Chapter II: Direct effects of Ponto-Caspian invasion on native parasites through the example of Pomphorhynchus sp. (Acanthocephala)……………….. 63 5 Pomphorhynchus laevis: An invasive species in the river Rhine?................... 64 5.1 Summary………………………………………………………………………….. 64 5.2 Introduction……………………………………………………………………….. 65 5.3 Material and methods……………………………………………………………. 69 5.4 Results…………………………………………………………………………….. 71 5.5 Discussion………………………………………………………………………… 74 Chapter III: Indirect effects of Ponto-Caspian invasion for local hosts through the example of an interaction between Pomphorhynchus laevis (Acanthocephala) and the invasive Anguillicola crassus (Nematoda)……………………………….. 79 6 First evidence for a possible invasional meltdown among invasive fish parasites……………………………………………………………………………….. 80 6.1 Summary………………………………………………………………………….. 80 6.2 Introduction……………………………………………………………………….. 81 6.3 Material and methods……………………………………………………………. 83 6.4 Results…………………………………………………………………………….. 85 6.5 Discussion………………………………………………………………………… 86 7 General discussion…………………………………………………………………. 89 8 References………………………………………………………………………….. 94 Appendices……………………………………………………………………………. 121 Appendix 1…………………………………………………………………….. 121 Appendix 2…………………………………………………………………….. 125 Contributions………………………………………………………………………….. 129 Curriculum vitae……………………………………………………………………… 130 Erklärungen…………………………………………………………………………… 133 List of abbreviations bp base pair CH Switzerland CO1 (genes) cytochrome c oxidase subunit I DCF data collection framework dpi days post infection IMH invasional meltdwon hypothesis IUCN International Union for Conservation of Nature ITS (genes) internal transcribed spacer L2 / L3 larvae stage 2 / 3 MDS multidimensional scaling MI mean intensity MQ mean water discharge N / n total number NIS nonindigenous species NL the Netherlands P prevalence PC Ponto-Caspian PCR polymerase chain reaction rpm revolutions per minute SD standard deviation sp. / spec. species 8 List of figures Figure 2.1: Hypothetical example of three possible scenarios that might take place after an invasive host enters a new environment: parasite spillback, spill over, and dilution effect……………………………… 22 Figure 3.1: Map of all sampling locations indicating all different sampling periods…………………………………………………………………. 28 Figure 3.2: Display of the final PCR-products after an agarose gel/ethidium bromide electrophoresis (including positive control of both Pomphorhynchus species; negative control). PCR- products with a length of 320 bp = P. laevis; 350 bp = P. tereticollis…………….. 31 Figure 3.3: Experimental setup of the artificial digestive process…………...... 32 Figure 4.1: Sampling locations: A = Rhine River at the city of Grieth; B = Ems River at the city of Ditzum; C = Elbe River at the city of Winsen a. d. Luhe, D = Schwentine River, close to the Großer Plöner See…. 41 Figure 4.2: Distribution of species richness in the parasite infracommunities of the three different fish species (A) G. cernua; B) N. melanostomus; C) A. anguilla) within the four German rivers (blue = Rhine; orange = Ems; gray = Elbe; yellow = Schwentine)………. 48 Figure 4.3: Internal parasite community of A) G. cernua; B) N. melanostomus; C) A. anguilla within the tested rivers (Rhine; Ems; Elbe; Schwentine)…………………………………………………………… 51 Figure 5.1a: Map of Europe, countries of interest highlighted in green………... 70 9 Figure 5.1b: Map of the sampling spots in the Rhine at Beneden Leeuwen (Netherlands), Karlsruhe (Germany) and Laufenburg (Switzerland)………………………………………………………….. 70 Figure 5.2: Sampling years (a = 2003, b = 2004, c = 2015), and Pomphorhynchus species distribution from eel at the three different sampling locations within the river Rhine [the Netherlands, Germany, Switzerland]……………………………….. 72 Figure 6.1a: Cysts of encapsulated P. laevis individuals as detected and removed from the digestive tracts of N. melanostomus…………… 85 Figure 6.1b: Encapsulated P. laevis irradiated with high light intensity………... 85 Figure 6.1c: Digested cyst with released A. crassus individuals……………….. 85 Figure 7.1: Graphical illustration of the three presented scenarios that follow a Ponto-Caspian invasion. Scenario: A) parasite spillback/spillover, B) extinction of native parasites, C) enhancement of local parasites through new transmission pathways………………………………………………………………. 91 10 List of tables Table 3.1: Account of all sampling locations (GPS-Coordinates) including the general information (primary source, river mouth, river basin, and mean discharge) of each river……………………………………….. 26 Table 3.2: Sampled host species with corresponding sampling locations and number sampled for the
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