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All issues No 422 (2021) Knowl. Manag. Aquat. Ecosyst., 422 (2021) 15 Full HTML
Open Access
Issue
Knowl. Manag. Aquat. Ecosyst.
Number 422, 2021
Article Number 15
Number of page(s) 8
DOI https://doi.org/10.1051/kmae/2021014
Published online 30 March 2021

© E. Żbikowska et al., Published by EDP Sciences 2021

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (https://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

Our research has focused on how the presence of a non-host snail species in the environment disturbs the transmission of bird schistosomes (Schistosomatidae, Digenea), zoonotic parasites whose larvae can penetrate the human skin. In the literature, there are numerous reports on the occurrence of a persistently itchy rash known as swimmer's itch (cercarial dermatitis) that appear after penetration of cercariae of parasite species belonging to the genera Trichobilharzia, Bilharziella, Allobilharzia into the skin of people wading in water reservoirs (Żbikowska et al., 2001; Żbikowska, 2004; Jouet et al., 2008; Lawton et al., 2014; Horák et al., 2015; Marszewska et al., 2016; Selbach et al., 2016; Caron et al., 2017; Marszewska et al., 2018; Liberato et al., 2019; Tracz et al., 2019). The attempts to control swimmer's itch on the etiology of bird schistosomes, in particular in Europe and America, are mainly undertaken in bathing areas where omissions regarding biological health hazards may result in economic losses to owners and managers of recreation alplaces (Soldánová et al., 2013). Snails are the target group of organisms against which efforts are directed to reducethe risk of infection (King and Bertsch, 2015). In the life cycle of all schistosomes, including those that infect birds, snails play the role of intermediate hosts and are crucial for the transmission of the parasites (Huot et al., 2020). Host snails are actively infected by ciliated miracidia hatching from the eggs, which find the host by chemoreception. The invasive larva penetrates the snail tegument and transforms inside the host into a mother sporocyst (Allan et al., 2009). In mother sporocysts, daughter sporocysts are formed, and inside them − cercariae invasive for final or accidental hosts develop. The total number of cercariae released from the snail during months of infection reaches values from several to several hundred thousands (Thieltges et al., 2008; Braun et al., 2018). The risk of swimmer's itch depends on the presence of snails infected with bird schistosome larvae in an environment. Even low prevalence (less than 10%) in snail populations is sufficient for the high risk of cercarial dermatitis (Soldánová et al., 2013). The control of human schistosomiasis is sometimes achieved by exterminating the host snails in the environment (Nelwan, 2019). Apart from the use of molluscicides, the methods of biological control of parasitic infections, such as dilution effect, deserve special attention (Johnson and Thieltges, 2010). Dilution effect means the decrease of infection levels in host population by competitors that reduce the host density. However, opponents of this method emphasize the lack of its universality (Civitello et al., 2015), but followers of introducing non-host species of snails into ecosystems to reduce parasite transmission underline that wherever it brings the expected positive effects − it should be used (Johnson et al., 2009).

1.1 Community diversity can mediate infection levels and disease

The choice of the species expected to produce a dilution effect and to decrease the transmission of parasites is crucial. Introduced snails should act as “dead-end” hosts or to be effective competitors for the natural hosts. The choice of some alien species in the controlled areas is one of the proposed ideas (Pointier and Jourdane, 2000).

The issue of the alien species has been one of the most common research trends in the recent literature (Da Silva et al., 2019; Rachalewski, 2019; Arumugam et al., 2020; Jermacz et al., 2020; Kondakov et al., 2020; Larson et al., 2020). The scientific focus on the research concerning the threat to native communities from alien fauna often results in overlooking their potential positive impacts (Goodenough, 2010). An example of an alien species considered to have a negative effect on native communities is the New Zealand mud snail (NZMS) − Potamopyrgus antipodarum (Gray, 1843) (Caenogastropoda, Hydrobioidea, Tateidae) (Brown et al., 2008). However, P. antipodarum exhibits parthenogenetic reproduction, resulting in extremely high population density, reaching many thousands of individuals per square meter, and it seems to be a better “dead-end” host for bird schistosomes than native non-host snail species (Brown et al., 1988; Hall et al., 2003; Levri et al., 2007; Davidson et al., 2008). According to these researchers, the species affects the consumption of a large part of primary production in ecosystems. The high effectiveness of P. antipodarum in the new areas is due to their high dietary and other phenotypic plasticity, including a generalist diet that comprises periphyton, diatoms, as well as plant and animal detritus. This feature makes this species a very effective competitor of other benthic invertebrates (Levri et al., 2007; Alonso and Castro-Díez, 2008; Brown et al., 2008).

The high population density of P. antipodarumas a non-native species has led some authors to the conclusion that this species contributes to a dangerous change in the community structure of water ecosystems (Gérard et al., 2003; Kerans et al., 2005; Brown et al., 2008; Lysne and Koetsier, 2008). However, it should be noted that the European populations of this species are characterised by large density fluctuations, which significantly reduce their impact on native community. High density followed by local extinction(Moffitt and James, 2012) results from the low genetic diversity of P. antipodarum individuals (Dorgelo et al., 2014). The low diversity of P. antipodarum haplotypes as a non-native species has also implications for a parasitic invasion (Lively, 1987). Some authors highlighted the probable negative impact of P. antipodarum as the host of parasites in new-inhabited ecosystems (Morley, 2008). However, P. antipodarum in its native area is the first intermediate host for at least 20 species of highly host-specific trematode parasitic castrators (Hechinger, 2012), with the prevalence of trematodes varying among the snail populations from 9% to 80% (Winterbourn, 1973, 1974; Lively, 1987; King et al., 2011). In the areas outside New Zealand only few cases of the infection with cercariae or metacercariae in the snails have been reported (Larson and Krist, 2020).

Long-term monitoring of the parasitic infection of snails in the lakes of the Polish Lowlands and intensive annual surveys of the P. antipodarum populations in the post-mining tanks in Silesia, resulted in finding one individual infected with lophocercariae (Żbikowski and Żbikowska, 2009), five individuals infected with pre-adult forms of Aspidogasterconchicola and 39 snails infected with echinostome metacercariae (Cichy et al., 2017). Additionally, the experimental infection of this snail with the miracidia of Trichobilharzia spp. conducted in our laboratory was unsuccessful (Marszewska et al., 2018, 2020). These data have indicated that the threat concerning the host role of P. antipodarum in European waters (Morley, 2008) is highly exaggerated. The alien species can both negatively and positively affect the native species by influencing parasite-host dynamics and disease occurrence (Kopp and Jokela, 2007; Marszewska et al., 2018; Goedknegt et al., 2019). Moreover, these authors have highlighted that there is surprisingly little research on the impact of the alien species on the parasite infection patterns in the native host communities (Goedknegt et al., 2019). They have also emphasised that the large-scale field studies are favourable for the detailed assessment of the aforementioned mechanism.

As a result ofthedilution effect created by increasing the diversity of co-occurring potential targets, the risk of various parasitic diseases may be reduced (Keesing et al., 2006; Kopp and Jokela, 2007; Cichy et al., 2017). Non-native species (i.e., P. antipodarum) seem to be good potential targets for creating a dilution effect because they lack natural enemies in the habitats.

The aim of this study was to check if there is arelationship between the presence of P. antipodarum and the infection of bird schistosomes in Lymnaea stagnalis (Linnaeus, 1758) populations in lakes of Polish Lowland. On the basis of long-term field study, we tested the hypothesis that an alien to Europe, such as P. antipodarum, has the potential for abiological control of swimmer's itch in recreational bathing areas.

2 Material and methods

2.1 Snail sampling and laboratory study

The material used for the parasitological studies were L. stagnalis specimens from 30 lakes in the Polish Lowlands inhabited and uninhabited by P. antipodarum (Fig. 1, SM 1). No empty shells of P. antipodarum in lakes uninhabited by this snail indicates that the lack of its individuals was not the result of local extinction (SM 1). Lymnaea stagnalis or P. antipodarum were dominant in the malacofauna of the studied sites. Snails, for parasitological diagnostic were collected manually only five times in each lake −from May to September between 2002 and 2019. Along with the acquisition of the malacological material for the parasitological studies, the presence of the invasion of the alien P. antipodarum in all sampling locations was verified. For this purpose, a semi-quantitative method was used, which was carried out with a 25 cm dredge. The samples from the area of 0.25 m × 0.25 m were taken three times in each lake during each sampling period.

During the snail sampling in most water bodies, the measurements of basic environmental parameters were made applying the MultiLine P4 (WTW) Universal Pocket Sized Meter. The pH, conductivity, water temperature and the oxygen content were measured. The characteristics of the lakes have been presented in Table 1 and SM 1.

A single malacological sample for parasitological diagnostics comprised at least 25 individuals of L. stagnalis. All of them were tested by standard procedures according to Blankespoor and Reimink (1991). The species of the recorded cercariae were determined on the basis of the morphological and anatomical characteristics (Cichy and Żbikowska, 2016).

thumbnail Fig. 1

Map of study lakes in the Polish Lowlands.
Table 1

GPS of the sampling area, year of research and physicochemical characteristics of investigated water reservoirs.

2.2 Statistical analysis

The Shannon-Wiener Index (H') was applied to calculate the species diversity of digeneantrematodes in L. stagnalis individuals from the lakes inhabited and uninhabited by P. antipodarum.

Due to strong deviations of our data from the assumption of normality and homoscedascity (high variation at zero density of NZM and lower at its higher densities) non-parametric Spearman correlation coefficient was used to check the relationship between NZMS density and the prevalence of digenean trematodes as well as between NZMS density and the prevalence of bird schistosomes.

The χ2 test of the contingency table was applied to compare the number of the lakes inhabited and uninhabited by P. antipodarum in terms of lymnaeid snails infected and non-infected by bird schistosomes. All the analyses were performed with PAST Statistical Software Package version 3.0 (Hammer et al., 2001). Statistical significance was assumed for p < 0.05.

The term “total infection” was used as a percentage of all L. stagnalis individuals infected with the digenean species in relation to all the individuals collected, whereas the term “prevalence” was used as a percentage of lymnaeid individuals infected with one digenean trematode species collected from one lake.

3 Results

In the study, 17 lakes without P. antipodarum and 13 lakes with P. antipodarum were investigated. A total of 4994 individuals of L. stagnalis were collected from all the studied lakes, 2231 and 2763 of which came from the lakes inhabited and uninhabited by P. antipodarum, respectively.

Snails infected with digenean trematodes were found in all the lakes, with the total infection of 34.2%. The infection of digenean trematodes in L. stagnalis from the lakes inhabited and uninhabited by P. antipodarum ranged from 16.4% to 51.2% (with the total infection of 32.4%) and from 19.8% to 64.8% (with the total infection of 35.7%) per lake, respectively (Fig. 2). There was no correlation in the infection of all the digenean species between the lakes inhabited and uninhabited by P. antipodarum (p = −0.21, t28 = 1.13, p = 0.270).

Seventeen species of digenean trematodes were found. The Shannon index showed no difference between the studied groups of water reservoirs in terms of the parasite species diversity (Tab. 2).

A significant difference in the number of reservoirs inhabited by snails infected with bird schistosomes was determined in the studied groups of water bodies (Fig. 2; χ2 = 5.43; df =1; p = 0.02). The bird schistosome infection was found in five lakes inhabited and 11 lakes uninhabited by P. antipodarum. The total infection of bird schistosomes was 1.4% in L. stagnalis from all the investigated water bodies, 0.3% from the lakes inhabited and 2.2% from the lakes uninhabited by P. antipodarum. Their prevalence ranged from 0 up to 1.2% and from 0 upto 10% in the lakes inhabited and uninhabited by P. antipodarum, respectively (Fig. 2), and was negatively correlated with NZMS density (p = −0.47, t28 = 2.83, P = 0.009) (Fig. 2).

thumbnail Fig. 2

Potamopyrgus antipodarum population density, total infection and bird schistosome prevalence in Lymnaea stagnalis populations at sampling sites in lakes: 1–Bielkowskie, 2–Czartek, 3–Czerwica, 4–BielczyńskieGłuchowskie, 5–Jelenieckie, 6–Ostrowąskie, 7–WielkiePartęczyny, 8–Pod Zamkiem, 9–Popek, 10–RudnickieWielkie, 11–Skulsk, 12–SkulskaWieś, 13–Służewskie, 14–Szymbarskie, 15–Tynwałdzkie, 16–WysokieBrodno, 17–Zielone, 18–Głuszyńskie, 19–ZalewPiechota, 20–Borówno, 21–Sobiejuskie, 22–Czarne, 23–NiskieBrodno, 24–BytyńWielki, 25–Iławskie, 26–Sendeńskie, 27–Górskie, 28–Wąsoskie, 29–Sosno, 30–Soczewka.
Table 2

Species diversity of Digenea in the studied populations of Lymnaea stagnalis.

4 Discussion

The presence of P. antipodarum in the lakes did not significantly affect the total digenean trematodes infection of the L. stagnalis populations; only in five out of 13 lakes the infection prevalence exceeded 30%, while in the lakes not inhabited by the alien snail species more than 30% infection was recorded in nine out of 17 subjects (Fig. 2). Given that themiracidia of flukes use chemoreception to find the snail host (Haas et al., 1995), it should be assumed that the chemoreception efficiency of most of the detected parasite species was high, regardless of the presence of P. antipodarum in the environment.

The Shannon diversity index of trematode parasiteswas similar in both types of lakes, and the only bird schistosome species found was Trichobilharzi aszidati (Neuhaus, 1952). However, it is noteworthy that T. szidati-infected snails were mainly present in the lakes uninhabited by P. antipodarum (Fig. 2). The similar physicochemical and biocenotic conditions in both groups of lakes (SM 1) suggest that the presence of P. antipodarum may be an important factor differentiating the occurrence of T. szidati larvae in L. stagnalis populations. The prevalence of the parasite in the host snailswith one exception did not exceed 5.5%. A small number of snails infected with bird schistosome in the studied lakes was in line with several earlier studies (Loy and Haas, 2001; Żbikowska, 2004; Jouet et al., 2008; Horák et al., 2015). It cannot be ruled out that the presence of non-host snail species in the environment generally disturbs the transmission of bird schistosome affecting a very low prevalence of the parasite. However, a high density of P. antipodarum populations could significantly disturb thistransmission. The fact that snails infected with T. szidati originated mainly from the lakes uninhabited by P. antipodarum may be due to the disturbance in the chemokinetic reaction of its miracidia by substances from the alien occurring at high population densities. The complicated behaviour of schistosome miracidia was studied in the 1960s by MacInnis (1965) and Wright and Ross (1966). The further research on testing of signal compounds has revealed that attractants for parasite larvae include both host-derived and non-host molecules (Allan et al., 2009). Marszewska et al. (2020) found that excretory-secretory products derived from P. antipodarum effectively disrupt the chemokinetic reaction of T. szidati miracidia. Given that miracidia have only one attempt in adhesion to the signal source (Haas et al., 1995), the contact of larvae with the wrong target (i.e., P. antipodarum) irreversibly ends the transmission of the parasite. Miracidia within an incompatible snail are eliminated by its hemocytes and/or plasma factors (Bayne et al., 2001). In addition, it has been experimentally confirmed that the effect of P. antipodarum on the reduction of bird schistosomes prevalence increases as P. antipodarum density also increases (Marszewska et al., 2018). They examined the effectiveness of T. regenti invasion into Radix balthica (Linnaeus, 1758) (Gastropoda, Basommatophora, Lymnaeidae) co-occurring with the growing density of P. antipodarum populations.

On the other hand, Loy and Haas (2001), Żbikowska (2004), Jouet et al. (2008), and Horák et al. (2015)have agreed that even the low prevalence of the patent invasion of bird schistosomes in the host snail populations is a real threat of swimmer's itch for humans. This opinion has been based on the high productivity of cercariae inside an infected individual of snail (Horák et al., 2015), as well as on the observation that most infections are recorded during the summer, when recreational water use is highest (Żbikowska, 2004).

Previous laboratory tests showed that the average number of cercariae released from one snail per (one) day exceeded even 1800 larvae (Żbikowska and Marszewska, 2018). The effectiveness of attacks of bird schistosomecercariae on humans was also high. Żbikowska et al. (2001) presented in detail the changes on the researcher's skin resulting from the penetration of a single or several cercariae during the collection of the field samples.

In light of the results obtained, suggestions for the use of the non-host species of snails for the biological control of parasites seems to be well justified. Of course, introducing non-native species even only on bathing waters requires a detailed analysis of the potential consequences. In the case of Schistosoma mansoni, which is responsible for severe human schistosomiasis, this control model exhibited the expected effects (Pointier et al., 2011). In the case of threat of swimmer's itch, the decrease in the prevalence of parasites due to the intentional introduction of non-host P. antipodarum into the bathing areas seems to be the form of protection that is worth considering. However, the ecological safety of such activities must be carefully examined and is the subject of ongoing research.

Conflict of interest

None of the authors of this paper has a financial or personal relationship with other people or organizations that could inappropriately influence or bias the content of the paper

Supplementary Material

SM 1 Table. Bottom type and biocenotic characteristics of sampling sites.

SM 2 Figure. Microscopical picture of the Trichobilharzia szidati cercaria.

Access here

Acknowledgements

This project was supported by the Biological and Veterinary Sciences of Nicolaus Copernicus University [statutory fund research], the Scholarships for PhD students − ZPORR − No. SPS.IV.0724-431/2010, and the grant of the National Science Centre, Poland No. 2017/25/N/NZ8/01345.

We would like to thank Paola Lombardo for proofreading an English version of the manuscript.

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Cite this article as: Żbikowska E, Stanicka A, Cichy A, Żbikowski J. 2021. Can Potamopyrgus antipodarum (Gastropoda) affect the prevalence of Trichobilharzia szidati in Lymnaea stagnalis populations? Knowl. Manag. Aquat. Ecosyst., 422, 15.

All Tables

Table 1

GPS of the sampling area, year of research and physicochemical characteristics of investigated water reservoirs.

In the text
Table 2

Species diversity of Digenea in the studied populations of Lymnaea stagnalis.

In the text

All Figures

thumbnail Fig. 1

Map of study lakes in the Polish Lowlands.
In the text
thumbnail Fig. 2

Potamopyrgus antipodarum population density, total infection and bird schistosome prevalence in Lymnaea stagnalis populations at sampling sites in lakes: 1–Bielkowskie, 2–Czartek, 3–Czerwica, 4–BielczyńskieGłuchowskie, 5–Jelenieckie, 6–Ostrowąskie, 7–WielkiePartęczyny, 8–Pod Zamkiem, 9–Popek, 10–RudnickieWielkie, 11–Skulsk, 12–SkulskaWieś, 13–Służewskie, 14–Szymbarskie, 15–Tynwałdzkie, 16–WysokieBrodno, 17–Zielone, 18–Głuszyńskie, 19–ZalewPiechota, 20–Borówno, 21–Sobiejuskie, 22–Czarne, 23–NiskieBrodno, 24–BytyńWielki, 25–Iławskie, 26–Sendeńskie, 27–Górskie, 28–Wąsoskie, 29–Sosno, 30–Soczewka.
In the text

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