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Host-Parasite Interactions in the European Shore Crab Carcinus Maenas and Their Implications for the Invasion Success of This Introduced Species

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Host-Parasite Interactions in the European Shore Crab Carcinus Maenas and Their Implications for the Invasion Success of This Introduced Species Host-parasite interactions in the European shore crab Carcinus maenas and their implications for the invasion success of this introduced species. Zur Erlangung des akademischen Grades eines DOKTORS DER NATURWISSENSCHAFTEN (Dr. rer. nat.) von der Fakultät für Chemie- und Biowissenschaften des Karlsruher Institut für Technologie (KIT) - Universitätsbereich genehmigte DISSERTATION von Dipl. Biol. Claudia Zetlmeisl geboren in Mannheim Dekan: Prof. Dr. Stefan Bräse Referent: Prof. Dr. Horst Taraschewski Korreferent: Prof. Dr. Bernd Sures Tag der mündlichen Prüfung: 12.07.2011 In memory of my father. Abstract As a consequence of globalisation and worldwide trade, invasive species increasingly pose a problem for ecologists and conservationists. In the invasive European shore crab Carcinus maenas , parasite loss during introduction was suggested to be a main reason for invasion success (parasite release hypothesis, PRH), based on observations of a correlation between crab mean size and biomass and the prevalence of parasitic castrators in Europe. This study aimed at further investigating this claim by examining host-parasite interactions of C. maenas and their consequences on individual fitness, with a focus on reproductive potential and immunological factors. To accomplish this, I examined crabs from a number of European populations, as well as from invasive populations in South Africa and Australia. My parasitological investigations showed that the source of invasive populations of this crab is an important factor for the consideration of the PRH, as parasite prevalence and intensity is highly variable, even on small scale geological distances, within Europe. However, my results on reproductive potential and on immune parameters of the hemolymph lend little further support to the PRH hypothesis. Parasitic castrators had a clear effect on reproduction, but apart from that the crabs were mostly unaffected by parasites, both on the individual level and the population level. There was weak evidence for an effect of microphallid parasites on hemocyte concentration under the influence of secondary stressors. Analysis of the age-intensity relation of helminths indicated that high intensities may lead to mortality in the crab hosts. Experimental infections with microphallids did not confirm these findings, but reduced hemolymph protein levels in infected crabs indicates that fresh infections strain the hosts metabolism and lead to a slight nutrient deficit. Based on these results, I suggest that parasites are not the major factor controlling or regulating C. maenas populations in Europe. It is more likely that multiple factors act on them, including chemical and physical characteristics of the environment, as well as community interactions. A loss of parasites during the invasion process may therefore contribute to the success of the shore crab as an invader, but it is unlikely to play a major role. Resource availability, community interactions or temperature regime in the invaded ecosystems could also be of relevance. In addition, my study focused on the effect of macroparasites, but the role of microparasites and other pathogens for C. maenas is largely unknown. Research into these areas may yield more information about the invasion success and may help to find new control measures against this invasive species. Zusammenfassung Invasive Arten stellen zunehmend eine Gefahr für die weltweite Biodiversität dar. Häufig wird der Invasionserfolg solcher Arten dem Fehlen natürlicher Feinde im neuen Lebensraum zugeschrieben. Zu diesen gehören auch Parasiten, wie im Fall der invasiven europäischen Strandkrabbe Carcinus maenas . Für diese Art wurde ein Zusammenhang von Durchschnittsgröße und Biomasse einer Population mit der Prävalenz von parasitischen Kastratoren festgestellt. Ziel meines Promotionsprojektes war es, die Rolle von Parasiten - und deren Fehlen - für den Invasionserfolg der Krabbe zu untersuchen. Zu diesem Zweck wurden Krabben aus Europa und aus den kolonisierten Gebieten in Australien und Südafrika auf Parasiten untersucht, sowie auf deren Auswirkungen auf die Fitness des Wirtes. Hierbei wurde besonderes Augenmerk auf das reproduktive Potential und auf Immunfaktoren gelegt, die als Fitnessindikatoren dienen. Meine Untersuchungen zeigen eine starke Variation sowohl in Bezug auf die Prävalenz als auch die Intensität von Parasiten in Europa. Aus diesem Grund spielt die Ursprungspopulation eine große Rolle bei der Beurteilung der Bedeutung von Parasitenverlust für den Invasionserfolg. Ich konnte bestätigen, dass parasitische Kastratoren den erwarteten negativen Effekt auf die Wirtsreproduktion haben. Was jedoch andere Parasiten sowie andere Fitnessparameter betrifft, konnte ich im Großen und Ganzen keine weiteren negativen Auswirkungen feststellen, weder in individuellen betroffenen Krabben noch auf Populationsebene. Es gab jedoch schwache Hinweise auf Mortalität bei starken Infektionen mit microphalliden Digenea sowie Anzeichen für Veränderungen in der Hämocytenkonzentration unter dem Einfluss von sekundären Stressoren. Experimentelle Infektionen mit diesen Parasiten konnten diese Beobachtungen nicht bestätigen, erniedrigte Proteinkonzentrationen in der Hämolymphe deuteten hier jedoch darauf hin, dass die generelle Konstitution des Wirtes beeinträchtigt wird. Zusammenfassend kann aus meinen Ergebnissen geschlossen werden, dass Parasitenbefall nicht der Hauptfaktor ist, der die Populationen von C. maenas in Europe kontrolliert. Es ist wahrscheinlich, dass zahlreiche Faktoren sowohl abiotischer als auch biotischer Art zusammenwirken. Daher ist davon auszugehen dass der Verlust von Parasiten im Verlauf des Invasionsprozesses nur bedingt zum Erfolg der Strandkrabbe in Übersee beiträgt. Andere Faktoren, die bisher noch kaum untersucht wurden, sind die Verfügbarkeit von Ressourcen und die unterschiedlichen Temperaturverhältnisse. Darüber hinaus beschränkt sich meine Arbeit auf die Auswirkung von Makroparasiten. Auch die Untersuchung anderer Pathogene könnte daher Aufschluss geben über den Invasionserfolg der Art, sowie Möglichkeiten für die Kontrolle der invasiven Populationen eröffnen. Acknowledgements First of all, I am grateful to my supervisor, Prof. Horst Taraschewski, for providing me with my thesis project and for his support and advice. My sincere thanks also go to Dr. Trevor Petney, who was never too busy to offer me his expertise in statistics and experimental design or to comment on my scientific writings. I would also like to thank Judith Hermann for teaching me everything I needed to know about the handling and examination of my study animals and its parasites. This thesis would not have been possible without the help of many collaboration partners from both Europe and overseas. For this reason I would also like to thank the Danish Skaldyrcenter and its director Frans Hoyer for providing not only laboratory space and materials, but also advice and support for my work in Denmark. In particular, my thanks go to Finn Bak for supplying me with large amounts of shore crabs. In Australia, my work was enabled by the research group of Prof. Robin Gasser of the University of Melbourne. I would like to thank Dr. Nathan Bott and Dr. Bronwyn Campbell for their invaluable assistance on the sampling efforts. Prof. Charles Griffiths made my research at the University of Cape Town, South Africa, possible and I am indebted to him for providing laboratory space and materials as well as study animals for both the field study and the experimental approach. I would also like to thank Candice Lyons for catching and caring for crabs in Cape Town. At the Karlsruhe Institute of Technology, my work was greatly supported by my colleagues, Dr. Miriam Pfäffle, Alexandra Mücke, Urszula Weclawski and Jasmin Skuballa, who provided a wonderful working atmosphere for me and who graciously cared for study animals whenever I needed assistance. My thanks also go to Bärbel Seufert-Dausmann and Sabine Steinbach for their help with university bureaucracy and in the laboratory. My research was financially supported by the Landesgraduiertenförderung, the Deutsche Bundesstiftung Umwelt and the Deutscher Akademischer Auslandsdienst. I would like to thank these institutions for making this project possible. Lastly, I would like to thank my family for their patience and their emotional support over the last years. Contents 1 INTRODUCTION ..............................................................................1 1.1 Biological invasions and marine ecosystems 1 1.2 Parasites in invasion biology and ecology 3 1.3 Thesis goals 4 2 MATERIALS AND METHODS..........................................................8 2.1 Study animals 8 2.1.1 The European shore crab Carcinus maenas ...................................................... 8 2.1.1.1 Native range and invasions ............................................................................ 9 2.1.1.2 Ecology and life cycle....................................................................................10 2.1.2 Parasites of the European shore crab ...............................................................12 2.1.2.1 Sacculina carcini ...........................................................................................14 2.1.2.2 Portunion maenadis ......................................................................................15 2.1.2.3 Profilicollis botulus .........................................................................................16 2.1.2.4 Microphallid trematodes ................................................................................17
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