From degraded to near-natural water bodies: establishment, development, and indicator function of trematodes

Freshwater ecosystems are increasingly shaped by anthropogenic alteration, resulting in habitat degradation and ongoing biodiversity loss. Although protection and restoration efforts have increased substantially in recent years, the complex ecological interactions governing ecosystem degradation and recovery remain difficult to comprehensively assess. Traditionally, the ecological status of freshwater ecosystems is evaluated by monitoring free-living organisms, particularly benthic invertebrates and fish, which provide important but inherently limited perspectives on ecosystem condition. Parasites offer a complementary approach for ecological assessments of freshwater ecosystems, as they are closely linked to free-living biodiversity and exhibit distinct life-history strategies that can either enhance or constrain tolerance towards ecological degradation. In particular, heteroxenous and host-specialist parasites react sensitively to ecosystem changes, as they rely on distinct or multiple hosts and stable trophic interactions for life cycle completion, whereas monoxenous and generalist parasites are more likely to persist under degraded conditions. Digenean trematodes are particularly well suited for assessing ecological change in aquatic ecosystems, as they can integrate information across multiple host species, trophic levels, and temporal scales. Trematodes are thus increasingly applied as indicators of free-living species diversity and recovery in aquatic ecosystems. Studies from coastal ecosystems demonstrate that trematodes respond rapidly to restoration and reflect long-term ecosystem succession as well as (or, in some cases, better) than free-living organisms. In stream ecosystems, however, evaluation of trematodes amid ecological change remains limited, and their responses to freshwater degradation and recovery insufficiently understood. Accurate assessment of trematode responses critically depends on detailed knowledge of their life cycles, host specificity, and transmission strategies. Although around 18,000 trematode species have been formally described, complete life cycles are known for only a fraction, constraining both taxonomic resolution and ecological interpretation. Advances in molecular species identification have facilitated trematode life cycle reconstruction, and revealed extensive cryptic diversity within the Trematoda, highlighting the necessity of integrative species identification to reliably infer life-history strategies and draw accurate ecological conclusions. Accordingly, this thesis comprises four chapters that aim to advance our understanding of the establishment, development, and indicator function of trematodes across degraded and near-natural freshwaters. In Chapter I, recolonization and early establishment of trematodes is examined in a previously uninhabited river (Emscher, Germany) following large-scale stream restoration. Seasonal samplings of first intermediate snail hosts were conducted over two years postrestoration. The results of this chapter demonstrate rapid trematode recolonization and indicate that trematode establishment is primarily facilitated by introduction through mobile definitive hosts from the regional species pool, rather than by phylogenetic host specificity or life cycle complexity. The exclusive occurrence of allogenic trematode taxa suggests a key role of high dispersal capacity and flexible habitat use of definitive hosts during early phases of recovery. However, geographic host turnover within the observed phylogenetic ranges, the high contribution of taxa with truncated life cycles to overall prevalence, and the absence of clear successional trajectories underscore the complexity of trematode-host interactions in recovering ecosystems. Continued monitoring of the Emscher will be essential to evaluate how the relative importance of individual life-history traits shapes trematode succession over time. In Chapter II, successional trajectories of trematode communities are examined in an urban stream system with a history of severe degradation and gradual restoration (Boye, Germany), and related to restoration history and surrounding land-use patterns. Over two consecutive years of monthly sampling, 6,300 snails of 13 different species and 25 distinct trematode taxa were investigated. Adjacent land use emerged as a consistent predictor of trematode species richness and overall prevalence, with agricultural sites differing significantly from forested or urban habitats. Restoration history was not associated with changes in trematode assemblages, suggesting quick recovery of trematodes and hosts in recently restored habitats. The most abundant snail species, Ampullaceana balthica, was identified as a key host, harboring the majority of trematode taxa and the highest infection prevalence. These findings highlight land use as a dominant landscape-level driver of trematode dynamics in urban freshwater ecosystems and support trematodes as complementary bioindicators for the assessment of ecological conditions in restored streams. An example of the elucidation of complex trematode life cycles is provided in Chapter III, which examines the life cycles of two trematode taxa from freshwater ecosystems in southern Africa. The molecular identification of cercarial and metacercarial stages enabled species identification of two previously undescribed developmental stages in first intermediate snail hosts and second intermediate fish hosts. Cercariae and metacercariae of both lineages were morphologically examined and descriptions provided to support future species descriptions and applications in taxonomical or ecological studies. Based on these results, the life cycles of two trematode species were partially reconstructed. These findings expand current knowledge of diversity, host use, and life cycle strategies of trematodes, and highlight the importance of life cycle reconstruction for the application of trematodes as ecological or crosstaxon indicators. In Chapter IV, such life cycle knowledge was applied to investigate the diversity, prevalence, and the seasonality of transmission dynamics of amphibian-infecting trematodes via the first intermediate snail hosts. These results recover two potentially novel species of amphibian-infecting trematodes and demonstrate the value of using intermediate hosts to detect and assess trematodes of rare or protected hosts. As previous parasitological assessments were almost exclusively restricted to morphological species identification of adult trematodes in definitive hosts, future molecular matching to the now provided molecular sequences will be needed to unravel species identities, host use, and transmission strategies. The results of this thesis demonstrate that trematodes have considerable, yet insufficiently applied potential as ecological indicators in freshwater ecosystems. In particular, heteroxenous and host-specific trematodes have proven to be sensitive indicators of food web structure and stability, whereas generalist, monoxenous parasites persist even under degraded conditions. The findings of Chapters I and II show that trematodes respond to both large-scale land use gradients and restoration processes, with land use acting as a stronger driver than local restoration measures aimed at structural improvement. The rapid establishment of trematodes and the absence of clear succession patterns further indicate that recolonization is strongly dependent on the mobility of definitive hosts and an open regional species pool and cannot be inferred solely from life cycle complexity or host specificity. Chapters III and IV demonstrate that the ecological interpretation of trematode-specific patterns critically depends on reliable, integrative species identification. The combination of morphological and molecular characterization not only enables the assignment of previously unknown developmental stages and life cycles, but also reveals substantial cryptic diversity. Overall, this thesis shows that trematodes uniquely link parasitological and ecological research and can serve as an interface between host diversity, food web structure, and environmental changes. Methodologically, this thesis shows that robust ecological conclusions can only be drawn from an integrative approach combining long-term field studies, a differentiated consideration of land use and habitat quality, and modern molecular and morphological analyses. Thus, two key implications arise for future research and application: First, trematodes should be systematically integrated into monitoring and assessment programs for rivers and lakes, especially where traditional bioindicators reach their limits. Second, the continued expansion of well-referenced sequence data and resolved life cycles is essential to more widely apply trematodes as bioindicators and assess the role of parasites in degraded, restored and near-natural freshwater systems.