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Direct and Indirect Effects of Invasive Parasites on Native Blue Mussels

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Direct and Indirect Effects of Invasive Parasites on Native Blue Mussels Direct and indirect effects of invasive parasites on native blue mussels – Mytilicola intestinalis Steuer, 1902 affects its host Mytilus edulis Linnaeus, 1758 and modifies ecological interactions to other species in the Wadden Sea Dissertation zur Erlangung des Doktorgrades doctor rerum naturalium (Dr. rer. nat.) der Mathematisch-Naturwissenschaftlichen Fakultät der Christian-Albrechts-Universität zu Kiel vorgelegt von Felicitas Demann Kiel, 2018 Erster Gutachter: Dr. Mathias Wegner Zweiter Gutachter: Prof. Dr. Heinz Brendelberger Tag der mündlichen Prüfung: 26.04.2018 „Wenn Du fragst, was rechtes Wissen sei, so antworte ich, das, was zum Handeln befähigt.“ Hermann Ludwig Ferdinand von Helmholtz Contents Contents Zusammenfassung ............................................................................................................... - 5 - Summary .............................................................................................................................. - 7 - I. Introduction ................................................................................................................. - 9 - 1. Invasions in the German Wadden Sea & anthropogenic global change .................... - 9 - 2. Parasite-mediated direct and indirect effects of biological invasions ..................... - 11 - 3. The Mytilicola intestinalis – Mytilus edulis parasite-host system ......................... - 12 - 3.1. Bioinvasion of Mytilicola intestinalis .............................................................. - 12 - 3.2. Direct life cycle of Mytilicola intestinalis ........................................................ - 13 - 3.3. Within the host ................................................................................................. - 14 - 3.4. Movements in the host’s gut ............................................................................ - 15 - 3.5. Effect of M. intestinalis on its host .................................................................. - 16 - 4. Thesis outline ........................................................................................................... - 17 - II. Chapters I-III ................................................................................................................ - 23 - Chapter I ............................................................................................................................ - 25 - Chapter II ........................................................................................................................... - 47 - Chapter III ......................................................................................................................... - 63 - III. Conclusions and Perspectives ............................................................................... - 81 - References ........................................................................................................................... - 87 - Acknowledgements .......................................................................................................... - 103 - Affidavit ............................................................................................................................ - 105 - - 3 - - 4 - Zusammenfassung Zusammenfassung Mit der Zunahme biologischer Invasionen innerhalb des marinen Ökosystems wächst die Rolle von Parasiten in solchen Invasionsprozessen stetig. Wenn Parasiten selbst invasiv sind und auf heimische Arten überwechseln, können sie eine Reihe direkter und indirekter Effekte auf den neuen Wirt und die mit ihm interagierenden Arten ausüben. Direkte Effekte wirken auf vielfältige Weise auf den Wirt ein, daraus können wiederum indirekte Effekte hervorgehen. Indirekte Effekte können weiter auf die Interaktion zwischen Wirten und die mit ihnen wechselwirkenden Arten einwirken. Als Folge von beidem (direkten und indirekten Effekten) können Parasiten die Sensibilität eines Wirtes gegenüber weiteren Einflüssen, wie beispielsweise veränderten Klimabedingungen und/oder Sekundärinfektionen, beeinflussen. Dies hat tiefgreifende ökologische Auswirkungen für heimische Arten. Insgesamt bergen die Herausforderungen von Invasionsprozessen und dem Klimawandel das Risiko der Artenhomogenisierung und dem Aufkommen von Krankheiten. Vor diesem Hintergrund ist es eine der Hauptaufgaben der marinen Forschung zukünftige Einflüsse und Folgen von parasiten-beeinflussten Invasionen und dem Klimawandel abzuschätzen. In der vorliegenden Arbeit werden die direkten und indirekten Effekte des invasiven Parasiten Mytilicola intestinalis auf heimische Miesmuscheln untersucht. Die Arbeit gliedert sich in drei Kapitel, das erste Kapitel befasst sich mit den direkten Effekten, Kapitel zwei und drei mit den indirekten Effekten. Um die Auswirkungen von M. intestinalis auf heimische Miesmuscheln zu untersuchen, habe ich verschiedene Experimente auf der Insel Sylt (Deutsche Bucht, Nordsee) durchgeführt. Zunächst habe ich Miesmuscheln künstlich mit dem Darmparasiten infiziert, um die späteren experimentellen Daten unter Hinzunahme bekannter Infektionsintensitäten zu interpretieren. In unterschiedlichen Labor- und Feldexperimenten habe ich verschiedene direkte Effekte des invasiven Parasiten auf seinen Wirt analysiert. Diese Untersuchungen beziehen Experimente zu Isotopenwerten von Stickstoff (von Muscheln, Parasiten und Nahrungsressourcen) und den Stoffwechselprofilen von parasitierten und nicht-parasitierten Muscheln sowie deren Wachstum und Kondition mit ein (Kapitel I). Die Ergebnisse zeigen, dass die stabilen Stickstoffisotopenwerte für den Parasiten im Vergleich zum Wirt selbst, erhöht sind. Es wird deutlich, dass der Parasit hauptsächlich Gewebe des Wirtes konsumiert. Die direkte Aufnahme von Wirtsgewebe resultierte in einem veränderten Stoffwechselprofil für infizierte Muscheln, wobei hauptsächlich Stoffwechselprodukte des Aminosäurezyklus beeinträchtigt waren. Unter Feldbedingungen wuchsen experimentell infizierte Muscheln langsamer als nicht-infizierte Muscheln. Unter Laborbedingungen zeigten parasitierte Muscheln eine geringere Kondition als nicht-parasitierte Muscheln auf. Dies deutet auf einen direkten negativen Effekt des Parasiten auf seinen Wirt hin. Darüber hinaus habe ich eine Langzeitstudie (von Oktober 2014 bis September 2015) über die monatliche Parasiteninfektion einer intertidalen Miesmuschelbank durchgeführt. Mittels der bekannten Parasitenintensität können die experimentellen Momentaufnahmen der direkten Effekte über die - 5 - Zusammenfassung Jahreszeiten hinweg extrapoliert werden. Der saisonale Verlauf der Parasitenpopulation zeigte, dass eine permanente aber variierende Belastung der Muscheln mit dem Parasiten besteht. Jeweils im Sommer und im Herbst wurde ein Reproduktionspeak des Parasiten verzeichnet (Kapitel I). Neben den direkten Effekten habe ich die indirekten Effekte des Parasiten untersucht. Dazu habe ich die Räuber-Beute- Beziehung infizierter und uninfizierter Miesmuscheln zu einem ihrer Hauptprädatoren, der Strandkrabbe Carcinus maenas, analysiert. Dafür habe ich drei Prädationsexperimente entworfen, die ich mit zwei unterschiedlichen Lebensstadien des Parasiten im Labor durchgeführt habe (Kapitel II). Im Ergebnis wurde deutlich, dass der invasive Parasit indirekt die Räuber-Beute Beziehung von Muscheln und Strandkrabben beeinflusste. Der Prädationsdruck auf Wirte, die mit juvenilen Stadien des Parasiten infiziert waren, war niedrig, wohingegen dieser hoch war, wenn Wirte mit adulten Parasitenstadien infiziert waren. Dieses sich umkehrende Muster wurde zu verschiedenen Zeiten im Jahr deutlich, (Kapitel II). Schließlich habe ich krankheits-relevante Effekte des Parasiten auf die Immunantwort von Muscheln in einem Laborexperiment untersucht. Durch die Simulation verschiedener Infektionsszenarien habe ich den Krankheitsverlauf von parasitierten und nicht parasitierten Muscheln mit solchen verglichen, die zudem mit sekundären Vibrio spp. infiziert waren. Dazu habe ich die Phagozytoserate der Muschelhämozyten gemessen und die Vibriobelastung anhand der Kolonie bildenden Einheiten für die unterschiedlichen Infektionsansätze ermittelt. Dieses Experiment habe ich unter verschiedenen Temperaturkonditionen durchgeführt (Kapitel III). Das Infektionsexperiment zeigte, dass der invasive Parasit die Phagozytosekapazität von Muscheln beeinträchtigt, auch wenn dieser nicht direkt mit den Hämozyten der Muschel interagiert. Bei höheren Temperaturen führte dies zu einer erhöhten Anzahl Kolonie bildender Einheiten und dadurch zu einer erhöhten Mortalität von parasitierten Muscheln, die zusätzlich mit Vibrio spp. infiziert waren (Kapitel III). Indem ich die Ergebnisse verschiedener Labor- und Feldexperimente kombiniert habe konnte ich zeigen, dass der Parasit direkte und indirekte Effekte auf seinen Wirt ausübt. Eine Infektion mit dem Parasiten limitiert die verfügbaren Ressourcen für das Wachstum (direkte Effekte) aber auch für die Immunantwort von Miesmuscheln gegen sekundäre Infektionen (indirekte Effekte). Dies zeigt, dass direkte Effekte des Parasiten wiederum die Wechselwirkungen seines Wirtes zu dritten Arten verändern können. Die vom Lebensstadium des Parasiten abhängige Manipulation des Prädatorverhaltens repräsentiert einen extremen Fall von solchen indirekt veränderten Interaktionen. Dies verdeutlicht, dass indirekte Effekte das Ausmaß von direkten Effekten übertreffen können. Um die ökologischen Auswirkungen von biologischen Invasionen im Allgemeinen und die von invasiven Parasiten im Speziellen abschätzen
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