Direct and indirect effect of invasive parasites on native blue mussel hosts

Mathias.Wegner [ at ]


The role of parasites in invasion processes have become an increasing phenomenon due to the continuous increase in the rate of biological invasions in marine ecosystems. When parasites themselves are invasive and spill over to native species, they can exert a number of direct and indirect effects on their new host and interacting species. Direct effects often affect the new host in multiple ways that result in further indirect effects downstream. Moreover, the occurrence of indirect effects might change the interaction of the host to interacting species. As a result of both, direct and indirect effects, parasites can change the sensitivity of the host against further impacts like climate change and/or secondary infections. This can have profound ecological consequences for native biota. In combination, the challenges of invasion processes and climate change bear the risk of species homogenization and disease emergence. Against this background, it is an urgent task of marine science to assess future impacts and consequences of parasite invasions and climate change. The present study investigates the direct and indirect effects of the invasive parasite Mytilicola intestinalis on native blue mussels. The study is divided into three chapters; the first chapter addresses the direct effects, while the second and third chapter considers indirect effects. To investigate the impacts of M. intestinalis on native blue mussels, I conducted different experiments on the island Sylt (German Bight, North Sea). Initially, I experimentally infected mussels with the intestinal parasite to interpret experimental data in the light of known infection intensities. Thereafter, I investigated several direct effects of the invasive parasite on its host, in both field and laboratory studies. Those investigations include analyses on the nitrogen isotope values of mussels, parasites and food sources, experiments on the metabolic profile of parasitized and non-parasitized mussels, as well as their growth and condition (Chapter I). The results showed an enrichment of stable nitrogen isotopes in the parasite compared to the host indicating that the parasite primarily consumes host tissue. This direct consumption of host tissue further resulted in an altered metabolic profile with most metabolites of the amino acid cycle being affected. Under field conditions, experimentally infected mussels grew slower than non-infected mussels. Under laboratory conditions, parasitized mussels showed a lower condition than non-parasitized mussels, indicating a direct negative impact of the parasite on its host. Furthermore, I executed a long-term survey (from October 2014 to September 2015) on the monthly parasite infestation at an intertidal mussel bed. With the known parasite infection intensity background in the field, the experimental snapshots could be extrapolated across seasons. The seasonal course of the parasite’s population dynamics showed a distinct pattern with a permanent but varying burden of mussels by the parasite and the main parasite broods occurring in summer and autumn, (Chapter I). Next to these direct effects, I explored the indirect effects of the parasite. I looked at the predator-prey interaction of experimentally infected and uninfected blue mussels with one of their most prominent predators, the shore crab Carcinus maenas. To do so, I conducted three laboratory predation experiments that I carried out with two different life stages of the parasite (Chapter II). The invasive parasite indirectly influenced the predator-prey interaction of mussels and shore crabs. Initially, predation pressure on hosts infected with juvenile parasite stages was low, whereas, this pattern was reversed when crabs were offered mussels infected with adult parasite stages at a different time of the year (Chapter II). Finally, I investigated the trait-mediated effects of the parasite on the immune response of mussels to a secondary infection in a laboratory experiment. Simulating different infection scenarios, I compared the pathogenesis and immune response of parasitized and non-parasitized mussels to those that were additionally infected by secondary Vibrio spp. infections. For that purpose, I measured the phagocytosis rates of the mussel hemocytes and estimated the Vibrio load by evaluating the number of viable cells for the various infection treatments. This experiment was performed under different temperature conditions, (Chapter III). The infection experiment revealed that the invasive parasite limits the phagocytosis capacity of mussels without directly interacting with the hemocytes of the host. At higher temperatures, the decreased phagocytosis activity led to a higher Vibrio spp. load, resulting in an increased mortality of parasitized mussels when exposed to a secondary Vibrio spp. infection (Chapter III). Combining the results of laboratory and field experiments, I could show that an infection by the parasite M. intestinalis has various direct and indirect effects for the host. A parasite infection limits the resources available for growth (direct effects) but also for the immune response of mussels against secondary infections, (indirect effects). This demonstrates that direct effects of the parasite may indirectly modify the interaction of its host with third species. The life-stage dependent manipulation of predator behavior by the parasite represents an extreme case of such altered interactions and clearly shows that indirect effects can outweigh direct effects. Therefore, such indirect effects and their interactions with the biotic and abiotic environment need to be taken into account to fully assess the ecological consequences of biological invasions in general and parasitic invasions in particular.

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Thesis (PhD)
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Demann, F. (2018): Direct and indirect effect of invasive parasites on native blue mussel hosts , PhD thesis, University of Kiel.

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