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Biology and ecology of trematodes parasitizing aquatic snails in the Ruhr reservoir system in Germany

Selbach, Christian LSF

Parasites are integral and important elements of ecosystems that occur in virtually every habitat on this planet (Poulin 1999, Hudson et al. 2006). However, except for the obviously important role of some species as disease agents, parasites have long been neglected and considered unimportant in the context of most ecological studies. Only in recent years, studies have begun to investigate the ecological importance of parasites, e.g. their structuring forces in trophic transmissions and food webs (Lafferty et al. 2008) or their contribution to an ecosystem’s biomass (Kuris et al. 2008, Thieltges et al. 2008). It has been argued, that it is even impossible to fully understand ecosystems without considering the parasites therein (Lafferty et al. 2006a). Furthermore, based on their often complex life cycles and strong interaction in ecosystems, parasites may serve as useful bioindicators to assess environmental conditions and changes (Lafferty 1997, Vidal-Martínez et al. 2010, Nachev & Sures, 2015). Environmental changes, such as climate change and global warming are expected to have major impacts on parasites and on entire ecosystems, often with yet unpredictable consequences (Marcogliese 2001, 2008). It is, therefore, essential that we understand host-parasite systems at the ecosystem level. Although there are some exceptionally well-studied aquatic ecosystems that focus on the roles of parasites in these habitats and allow predictions of the impact and possible effects of environmental changes (e.g. Kuris et al. 2008, Preston et al. 2013, Thieltges et al. 2013, Lagrue et al. 2015), our knowledge of host-parasite interaction in man-made waterbodies, such as impounded lakes and reservoirs, is still very limited and large-scale studies focussing on the ecological role of parasites in such systems are lacking. This is especially critical, since such waterbodies fulfil vital roles in densely populated areas, where they serve as drinking water storages, recreational areas and constitute important biodiversity hot spots. The Ruhr area in Germany is one of the largest and most densely populated urban areas in Europe and the eponymous extensive reservoir system of the Ruhr and its tributaries plays a vital role for the whole region. Our knowledge of the ecological role of parasites in these aquatic habitats is still fairly limited, however. In order to bridge this gap, this thesis aims at assessing the biology and ecology of trematodes parasitizing aquatic snails in the Ruhr reservoir system in Germany. Trematodes in snails have been identified as a particularly promising group of parasites that lend themselves to investigating and assessing environmental conditions and ecosystem changes in aquatic systems (Huspeni & Lafferty 2004), due to their complex multiple-host life cycles that enable us to study the complex roles of parasites in ecosystems at many levels and in great detail. This thesis, therefore, aims at addressing the importance of trematodes in the Ruhr reservoir systems by identifying larval trematode infections in snails in the reservoirs of the Ruhr river system. The individual studies of this work provide (i) detailed integrative approaches to taxonomically questionable trematode groups to assess the full diversity in the ecosystem, (ii) an analysis of the productivity and emergence of trematode cercariae to assess the parasites’ functional role in the ecosystem, (iii) an evaluation of the risk factors of swimmer’s itch via a detailed case study of one of the Ruhr lakes, and finally (iv) an assessment of the overall diversity, distribution and community structure of larval trematodes and the identification of potential trematode transmission pathways between their host groups. Altogether, this holistic approach, encompassing trematode taxonomy, their functional part in ecosystems, the role of medically relevant species and their contribution to an ecosystem’s diversity will provide a detailed and comprehensive insight into the complex role of trematodes in an important reservoir system in Europe. In order to assess the diversity and distribution patterns of trematodes in the Ruhr area, snails were collected at several sampling sites in five reservoirs of the Ruhr river catchment area in Germany, Baldeneysee, Hengsteysee, Hennetalsperre, Sorpetalsperre and Versetalsperre, during the summer months of the years 2012 and 2013. Sampling and analyses were mostly focused on gastropod snails belonging to two families, Lymaeidae and Planorbidae, since they proved to harbour the most diverse trematode fauna in Europe (Faltýnková & Haas 2006, Soldánová et al. 2011, Brown et al. 2011). A total of 3,171 lymnaeid snails belonging to four species, Radix auricularia, Stagnicola palustris, Radix peregra and Lymnaea stagnalis, and 2,176 planorbid snails belonging to two species, Gyraulus albus and Segmentina nitida, were collected and screened for trematode infections. Trematode stages were identified according to morphological features and, where necessary, with the aid of molecular methods. Of the 5,347 sampled snails, 1,049 showed patent or prepatent infections with trematodes, resulting in a total prevalence of 19.6%. Detailed integrative approaches of molecular and morphological methods revealed the presence of cryptic species within the trematode genera Echinostoma, Petasiger and Diplostomum. The analysis of Echinostoma spp. cercariae allowed the delineation of two cryptic species of the ‘revolutum’ group from larval stages found in R. auricularia, R. peregra and S. palustris. Likewise, analyses of infections from G. albus revealed the distinctive status of three species of Petasiger from this host that occurred in sympatry at one locality, highlighting the high diversity within this trematode genus, even at small spatial scales. Most distinctively, seven different species of Diplostomum were found in the lymnaeid snail populations from the Ruhr reservoirs, three named species, D. spathaceum, D. pseudospathaceum and D. parviventosum, and four species-level lineages, ‘Diplostomum sp. Clade Q’ and ‘D. mergi’ Lineages 2-4. Furthermore, the detailed approach provided evidence that the cercariae of ‘D. mergi’ Lineage 1 of Georgieva et al. (2013a) are actually D. parviventosum. Remarkably, the snail species L. stagnalis and S. palustris harboured only one species, D. pseudospathaceum, while R. auricularia populations revealed a highly diverse picture with six different lineages of Diplostomum, and it remains to be investigated why the diversity of Diplostomum in these hosts presents such contrary situation. Altogether, these integrative approaches of molecular and morphological data advance our knowledge of the taxonomic situation of these trematode taxa and reveal the remarkably high cryptic diversity of these parasites in the Ruhr reservoir system. However, the knowledge of the sheer diversity of trematodes in snails does not provide information on their functional role within an ecosystem. In order to assess the contribution of trematode cercariae to the biomass in European freshwaters, cercarial emergence of the bird schistosome Trichobilharzia szidati from naturally infected L. stagnalis was studied. The study revealed an average daily emergence rate of 2,621 cercariae per snail, with emissions peaks of up to 29,560 cercariae. Calculated for an individual snail’s lifetime this summed up to a cumulative cercarial biomass of 4.8 g, a mass equivalent of or even exceeding the snail‘s own body weight, illustrating the ecological importance a single trematode species that contributes a considerable amount of cercarial mass to an aquatic ecosystem. Since T. szidati is only one out of 37 species that produce large amounts of cercariae, the overall cercarial biomass emitted into the Ruhr reservoirs is comparable to the impressive numbers recently calculated for marine (Thieltges et al. 2008), estuary (Kuris et al. 2008) and North American freshwater ecosystems (Preston et al. 2013). The results of this study demonstrate how trematodes, despite their small individual size, significantly contribute to the biotic productivity in the Ruhr freshwater system. Since bird schistosomes are the causative agents of swimmer’s itch, a re-emerging disease in Europe (Soldánová et al. 2013), the disease risk factors in the Ruhr area based on the occurrence, distribution and biology of these parasites was assessed for one reservoir (Baldeneysee). Two bird schistosome species, Trichobilharzia franki and T. szidati, could be detected at several sampling sites in Baldeneysee, where abundant lymnaeid snail populations were present. Although these species showed only low prevalence, human infections are well possible, due to the high numbers of cercariae that can be released from individual infected snail hosts in short periods of time, as shown in the laboratory emission studies. With a total of 37 species, the trematode species richness in the Ruhr reservoir system was considerably higher than the trematode species richness in snail intermediate hosts described from most other well-studied ecosystems (e.g. Faltýnková 2005, Faltynkova & Haas 2006, Thieltges et al. 2006, Żbikowska 2007, Kuris et al. 2008, Lagrue & Poulin 2015). Altogether, Radix auricularia harboured by far the most prevalent, species rich and diverse trematode fauna of all studied hosts, supporting the assumption that R. auricularia plays the most important role in the life cycle of trematodes in large reservoirs and lakes, comparable to the dominant role of L. stagnalis described for small pond systems. Similarly, G. albus harboured more diverse and prevalent trematode communities compared to S. nitida, which contrasts with the situation observed for these two species in small ponds (Faltýnková et al. 2008a). The analysis of the data from the Ruhr, therefore, suggests a characteristic host-parasite dynamics in large reservoir systems. The majority of trematode species in the Ruhr requires fish-eating or anatid birds as final hosts and almost all trematode species have life cycles involving trophic transmission of the parasites to their respective final host, which provides information on trophic interactions and energy flow in the ecosystem. Since trematodes with trophic transmission strategies often directly or indirectly alter their host’s behaviour in order to facilitate transmission success to the next host (see e.g. Lafferty & Morris 1996), they actively shape the structure of food webs through which they are transmitted. Therefore, the rich and abundant trematode fauna in the Ruhr freshwaters plays a highly complex role in the food web connectivity in the Ruhr reservoirs. Overall, the selected aspects of trematodes in the Ruhr river system studied in the context of this thesis provide a broad and comprehensive overview of these parasites in a freshwater ecosystem that is typical for freshwater reservoirs in Europe for the first time. Trematodes are deeply embedded in and active elements of the ecological processes that shape and structure ecological communities, energy flow and the biodiversity of complex ecosystems and the rich trematode fauna in the Ruhr contributes to key aspects that make this ecosystem more diverse, productive and stable, and thus healthy.

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Selbach, Christian: Biology and ecology of trematodes parasitizing aquatic snails in the Ruhr reservoir system in Germany. 2016.

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