Miroslava Soldánová

Swimmer's itch: etiology, impact, and risk factors in Europe

This review summarizes current knowledge about the occurrence and distribution of swimmers itch, with a focus on Europe. Although recent publications have reviewed the biology and systematics of bird schistosomes and their complex host-parasite interactions, the underlying ecological factors that create favorable conditions for the parasites and the way humans interact with infested water bodies require further attention. Relevant studies from the past decade were analyzed to reveal an almost complete set of ecological factors as a prerequisite for establishing the life cycle of bird schistosomes. Based on both records of the occurrence of the parasite infective agents, and epidemiological studies that investigate outbreaks of swimmers itch, this review concentrates on the risk factors for humans engaged in recreational water activities.

New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data

BackgroundThe digenean species of Echinostoma (Echinostomatidae) with 37 collar spines that comprise the so-called ‘revolutum’ species complex, qualify as cryptic due to the interspecific homogeneity of characters used to differentiate species. Only five species were considered valid in the most recent revision of the group but recent molecular studies have demonstrated a higher diversity within the group. In a study of the digeneans parasitising molluscs in central and northern Europe we found that Radix auricularia, R. peregra and Stagnicola palustris were infected with larval stages of two cryptic species of the ‘revolutum’ complex, one resembling E. revolutum and one undescribed species, Echinostoma sp. IG. This paper provides morphological and molecular evidence for their delimitation.MethodsTotals of 2,030 R. auricularia, 357 R. peregra and 577 S. palustris were collected in seven reservoirs of the River Ruhr catchment area in Germany and a total of 573 R. peregra was collected in five lakes in Iceland. Cercariae were examined and identified live and fixed in molecular grade ethanol for DNA isolation and in hot/cold 4% formaldehyde solution for obtaining measurements from fixed materials. Partial fragments of the mitochondrial gene nicotinamide adenine dinucleotide dehydrogenase subunit 1 (nad 1) were amplified for 14 isolates.ResultsDetailed examination of cercarial morphology allowed us to differentiate the cercariae of the two Echinostoma spp. of the ‘revolutum’ species complex. A total of 14 partial nad 1 sequences was generated and aligned with selected published sequences for eight species of the ‘revolutum’ species complex. Both NJ and BI analyses resulted in consensus trees with similar topologies in which the isolates from Europe formed strongly supported reciprocally monophyletic lineages. The analyses also provided evidence that North American isolates identified as E. revolutum represent another cryptic species of the ‘revolutum’ species complex.ConclusionOur findings highlight the need for further analyses of patterns of interspecific variation based on molecular and morphological evidence to enhance the re-evaluation of the species and advance our understanding of the relationships within the ‘revolutum’ group of Echinostoma.

Avian Schistosomes and Outbreaks of Cercarial Dermatitis

SUMMARY Cercarial dermatitis (swimmers itch) is a condition caused by infective larvae (cercariae) of a species-rich group of mammalian and avian schistosomes. Over the last decade, it has been reported in areas that previously had few or no cases of dermatitis and is thus considered an emerging disease. It is obvious that avian schistosomes are responsible for the majority of reported dermatitis outbreaks around the world, and thus they are the primary focus of this review. Although they infect humans, they do not mature and usually die in the skin. Experimental infections of avian schistosomes in mice show that in previously exposed hosts, there is a strong skin immune reaction that kills the schistosome. However, penetration of larvae into naive mice can result in temporary migration from the skin. This is of particular interest because the worms are able to migrate to different organs, for example, the lungs in the case of visceral schistosomes and the central nervous system in the case of nasal schistosomes. The risk of such migration and accompanying disorders needs to be clarified for humans and animals of interest (e.g., dogs). Herein we compiled the most comprehensive review of the diversity, immunology, and epidemiology of avian schistosomes causing cercarial dermatitis.

Integrative taxonomic approach to the cryptic diversity of Diplostomum spp. in lymnaeid snails from Europe with a focus on the ‘Diplostomum mergi’ species complex

BackgroundRecent molecular studies have discovered substantial unrecognised diversity within the genus Diplostomum in fish populations in Europe and North America including three species complexes. However, data from the first intermediate host populations are virtually lacking. This study addresses the application of an integrative taxonomic approach to the cryptic species diversity of Diplostomum spp. in natural lymnaeid snail populations in Europe with a focus on the ‘D. mergi’ species complex.MethodsTotals of 1,909 Radix auricularia, 349 Radix peregra, 668 Stagnicola palustris and 245 Lymnaea stagnalis were sampled at five reservoirs of the Ruhr river system in Germany and screened for infections with Diplostomum spp. Cercariae were examined and identified alive, fixed and under scanning electron microscopy. Sequences from the barcode region of the cytochrome c oxidase subunit 1 (cox1) mitochondrial gene and from the internal transcribed spacer cluster (ITS1-5.8S-ITS2) of the rRNA gene were amplified for 51 and 13 isolates, respectively.ResultsDetailed morphological and molecular analyses provided evidence for three named species (Diplostomum spathaceum, D. pseudospathaceum and D. parviventosum), and a further four species-level lineages (‘D. mergi Lineages 2–4’ and ‘Diplostomum sp. Clade Q’ in the lymnaeid snail populations from the Ruhr river basin. The paper provides the first descriptions of molecularly identified cercariae of D. spathaceum and of the cercariae of D. parviventosum, three lineages of the ‘D. mergi’ species complex and of ‘Diplostomum sp. Clade Q’.ConclusionThe integration of molecular and morphological evidence for Diplostomum spp. achieved in this study will serve as a baseline for species identification of these important parasites of snail and fish populations and thus advance further studies on the distribution of Diplostomum spp. in Europe.

Species diversity of Plagiorchis Lühe, 1899 (Digenea: Plagiorchiidae) in lymnaeid snails from freshwater ecosystems in central Europe revealed by molecules and morphology

Larval stages of Plagiorchis spp. are both ubiquitous and ecologically important parasites in snail populations of freshwater ecosystems in Europe. However, difficulties in distinguishing the morphologically similar cercariae used for species identification, may lead to underestimation of species diversity. In this study, 38 isolates of Plagiorchis spp. infecting two lymnaeid snails, Lymnaeastagnalis (L.) and Radix auricularia (L.), in five central European freshwater ecosystems were subjected to morphological and molecular assessment. Five morphologically homogeneous and genetically distinct lineages of Plagiorchis spp. were identified via matching molecular data for the mitochondrial cytochrome c oxidase subunit I (cox1) gene with detailed morphological and morphometric data of the cercariae. Comparative sequence analysis using partial 28S rDNA and ITS1-5.8S-ITS2 sequences revealed that three distinct cox1 lineages are conspecific with Plagiorchis elegans (Rudolphi, 1802), P. maculosus (Rudolphi, 1802) and P. koreanus Ogata, 1938, respectively, whereas the lineage identified based on cercarial morphology as P. neomidis Brendow, 1970 plus a single isolate that could not be assigned to a described species, did not match any of the available sequences for Plagiorchis spp. A key to the cercariae of Plagiorchis spp. parasitising lymnaeid populations in central Europe is provided to facilitate identification.

The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis

Digenean trematodes are common and abundant in aquatic habitats and their free-living larvae, the cercariae, have recently been recognized as important components of ecosystems in terms of comprising a significant proportion of biomass and in having a potentially strong influence on food web dynamics. One strategy to enhance their transmission success is to produce high numbers of cercariae which are available during the activity peak of the next host. In laboratory experiments with 13 Lymnaea stagnalis snails infected with Trichobilharzia szidati the average daily emergence rate per snail was determined as 2,621 cercariae, with a maximum of 29,560. During a snail’s lifetime this summed up to a mass equivalent of or even exceeding the snail’s own body mass. Extrapolated for the eutrophic pond where the snails were collected, annual T. szidati biomass may reach 4.65 tons, a value equivalent to a large Asian elephant. Emission peaks were observed after the onset of illumination, indicating emission synchronizing with the high morning activities of the definitive hosts, ducks. However, high cercarial emission is possible throughout the day under favorable lightning conditions. Therefore, although bird schistosomes, such as T. szidati constitute only a fraction of the diverse trematode communities in the studied aquatic ecosystem, their cercariae can still pose a considerable risk for humans of getting cercarial dermatitis (swimmers itch) due to the high number of cercariae emitted from infected snails.

Small-scale to large-scale and back: larval trematodes in Lymnaea stagnalis and Planorbarius corneus in Central Europe

We examined the small-scale temporal and spatial variability in composition and structure of larval trematode communities in Lymnaea stagnalis and Planorbarius corneus in two fish ponds in the Czech Republic and compared the patterns of richness and similarity to continental and regional trematode faunas of these hosts. The levels of parasitism in the populations of both hosts were high, the former parasitized predominantly by allogenic species maturing in a wide range of birds and the latter infected by relatively more species completing their life cycles in micromammals. Communities in both hosts exhibited a congruent pattern of seasonal change in overall infection rates and community composition with lower levels of infection in spring. Both temporal and spatial variation was closely related to the structure of snail populations, and no significant differentiation of community composition with respect to pond was observed. Comparisons with large-scale inventories revealed overall congruent patterns of decreased richness and similarity and increased variability at the smaller scales in both host–parasite systems. The relative compositional homogeneity of larval communities in both snail hosts irrespective of scale suggests that historical data at small to medium regional scales may provide useful estimates of past richness and composition of larval trematode communities in these snail hosts.

The Role of Spatial and Temporal Heterogeneity and Competition In Structuring Trematode Communities In the Great Pond Snail, Lymnaea stagnalis (L.)

Abstract: We assessed how spatial and temporal heterogeneity and competition structure larval trematode communities in the pulmonate snail Lymnaea stagnalis. To postulate a dominance hierarchy, mark-release-recapture was used to monitor replacements of trematode species within snails over time. In addition, we sampled the trematode community in snails in different ponds in 3 consecutive years. A total of 7,623 snails (10,382 capture events) was sampled in 7 fishponds in the Jindřichův Hradec and Třeboň areas in South Bohemia (Czech Republic) from August 2006 to October 2008. Overall, 39% of snails were infected by a community of 14 trematode species; 7% of snails were infected with more than 1 trematode species (constituting 16 double- and 4 triple-species combinations). Results of the null-model analyses suggested that spatial heterogeneity in recruitment among ponds isolated trematode species from each other, whereas seasonal pulses in recruitment increased species interactions in some ponds. Competitive exclusion among trematodes led to a rarity of multiple infections compared to null-model expectations. Competitive relationships among trematode species were hypothesized as a dominance hierarchy based on direct evidence of replacement and invasion and on indirect evidence. Seven top dominant species with putatively similar competitive abilities (6 rediae and 1 sporocyst species) reduced the prevalence of the other trematode species developing in sporocysts only.

Rapid colonisation of Lymnaea stagnalis by larval trematodes in eutrophic ponds in central Europe.

High recruitment rates of multiple species and hierarchical competition are the keys to a competitive exclusion model of community assembly in larval trematode communities in molluscs. Eutrophic environments provide conditions for accelerating trematode transmission and this would increase the strength of interspecific interactions. To test these predictions, we provide the first known assessment for a pulmonate snail host, and for highly productive aquatic environments, of the rates of colonisation and extinction at the level of individual snail host patches, of a large guild of trematode species. Using a uniquely large dataset from a relatively long-term mark-recapture study of Lymnaea stagnalis in six eutrophic fishponds in central Europe, we demonstrate extraordinarily rapid colonisation by trematodes of a snail host, thus meeting the assumptions of the competitive exclusion model. Overall annual colonisation rates ranged from 243% to 503% year(-1) so that the odds of trematode establishment in an individual snail in these ponds are two to five times per year. Extinction rates were substantially lower than colonisation rates and, therefore, would not result in turnover rates high enough to significantly affect prevalence patterns in the snail populations. At the species level, analyses of sample-based estimates of probabilities of colonisation revealed that shared species traits associated with transmission and competitive abilities determined the limits of colonisation abilities. Colonisation rates were exceedingly high for the species transmitted to the snails passively via eggs. There was a significant effect of species competitive abilities on colonisation rates due to subordinate species being substantially better colonisers than both strong and weak dominants, a pattern consistent with the predictions of the competition-colonisation trade-off hypothesis. Our results suggest that, with the extraordinarily high trematode colonisation potential in the area studied, the spatial and temporal patterns of intraspecific heterogeneity in recruitment may provide conditions for intensification of interspecific interactions so that complex community assembly rules may be involved.

Endoparasites of European perch Perca fluviatilis fry: role of spatial segregation

A total of 246 perch Perca fluviatilis L. fry, 20 to 106 d old from 3 different reservoir subpopulations (epipelagic perch fry, EPF; bathypelagic perch fry, BPF; littoral perch fry, LPF), were examined for parasites. Six species of endoparasites were found: the nematode Camallanus lacustris was the most common, followed by the cestodes Proteocephalus percae, Bothriocephalus claviceps, Glanitaenia osculata and the acanthocephalan Acanthocephalus lucii. All worms were juvenile or immature and were recovered from the intestinal lumen, with the exception of plerocercoids of Triaenophorus nodulosus, which were found in the body cavity or already encysted in the liver (the final site of infection of metacestodes). A marked difference was found in infection rates in the 3 spatially segregated subpopulations of perch fry. Parasites were found almost exclusively in LPF, which were heavily infected (overall prevalence = 30%) compared with the other studied subpopulations. Two species (C. lacustris and T. nodulosus) were found in 1 fish each (prevalence = 3%) in BPF, whereas EPF were uninfected. The species richness and prevalence of parasites in LPF increased from 20-24 d old fry (2 species of parasites; prevalence = 13%) to 106 d old fry (5 species of parasites; prevalence = 80%).