The impact of invasive Sinanodonta woodiana (Bivalvia, Unionidae) and mussel macroparasites on the egg distribution of parasitic bitterling fish in host mussels
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
2021/41/B/NZ8/02567
Narodowe Centrum Nauki
2021/41/B/NZ8/02567
Narodowe Centrum Nauki
2021/41/B/NZ8/02567
Narodowe Centrum Nauki
2021/41/B/NZ8/02567
Narodowe Centrum Nauki
2021/41/B/NZ8/02567
Narodowe Centrum Nauki
2021/41/B/NZ8/02567
Narodowe Centrum Nauki
2021/41/B/NZ8/02567
Narodowe Centrum Nauki
PubMed
40108247
PubMed Central
PMC11923366
DOI
10.1038/s41598-025-93717-8
PII: 10.1038/s41598-025-93717-8
Knihovny.cz E-zdroje
- Klíčová slova
- Freshwater mussel, Host selection, Host-parasite interactions, Invasive species, Mussel parasitism, Parasite facilitation,
- MeSH
- Cyprinidae parazitologie MeSH
- interakce hostitele a parazita * MeSH
- mlži parazitologie MeSH
- nemoci ryb parazitologie MeSH
- ovum MeSH
- Unionidae parazitologie MeSH
- zavlečené druhy * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
Facilitative and competitive interactions among coexisting parasite species, as well as among alternative host species, produce considerable ecological and evolutionary responses to host-parasite relationships. Such effects can be illuminated by impacts of non-native species on relationships in local communities. We used the association between parasitic European bitterling fish (Rhodeus amarus) and unionid mussels (which host bitterling eggs in their gills) to test the effects of the invasive Chinese pond mussel (Sinanodonta woodiana) and the presence of non-bitterling mussel macroparasites on the pattern of host mussel use by the bitterling across 12 unionid mussel communities with the absence or presence of S. woodiana (and variation in duration of coexistence with local species). While all six European mussel species were used by the bitterling (with the prevalence of > 30% in Unio spp.), no S. woodiana individual was infected by the bitterling. The presence of S. woodiana did not affect bitterling eggs distribution in native mussels. Large native mussels hosted more bitterling. Infection by non-bitterling parasites, mostly water mites (prevalence 47%) and trematodes (25%), did not affect rates of bitterling parasitism. We discuss our results in the context of the rapid evolution of non-native species in their new range and its implication on mussel conservation.
Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic
Institute of Vertebrate Biology Czech Academy of Science Brno Czech Republic
Modelling and Computational Science Lodz Centre for Analysis University of Lodz Lodz Poland
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Telfer, S. et al. Species interactions in a parasite community drive infection risk in a wildlife population. Science330, 243–246 (2010). PubMed PMC
Griffiths, E. C., Pedersen, A. B., Fenton, A. & Petchey, O. L. The nature and consequences of coinfection in humans. J. Infect.63, 200–206 (2011). PubMed PMC
Adegnika, A. A. & Kremsner, P. G. Epidemiology of malaria and helminth interaction: a review from 2001 to 2011. Curr. Opin. HIV AIDS. 7, 221–224 (2012). PubMed
Thumbi, S. M. et al. Parasite co-infections and their impact on survival of indigenous cattle. PLOS ONE. 9, e76324 (2014). PubMed PMC
Colwell, D. A., Wescott, R. B., Colwell, D. A. & Wescott, R. B. Prolongation of egg production of Nippostrongylus brasiliensis in mice concurrently infected with Nematospiroides dubius. J. Parasitol.59, 216–216 (1973). PubMed
Ezenwa, V. O., Etienne, R. S., Luikart, G., Beja-Pereira, A. & Jolles, A. E. Hidden consequences of living in a wormy world: Nematode‐induced immune suppression facilitates tuberculosis invasion in African Buffalo. Am. Nat.176, 613–624 (2010). PubMed
Rodgers, M. L. & Bolnick, D. I. Opening a can of worms: a test of the co-infection facilitation hypothesis. Oecologia204, 317–325 (2024). PubMed PMC
Bashey, F. Within-host competitive interactions as a mechanism for the maintenance of parasite diversity. Philos. Trans. R Soc. B-Biol Sci.370, 20140301 (2015). PubMed PMC
Sanad, M., Sun, J. S., Shamseldean, M. S. M., Wang, Y. & Gaugler, R. Superparasitism and population regulation of the mosquito-parasitic Mermithid nematodes Romanomermis iyengari and Strelkovimermis spiculatus. J. Nematol. 49, 168–176 (2017). PubMed PMC
Tripet, F. & Richner, H. Density-dependent processes in the population dynamics of a bird ectoparasite Ceratophyllus gallinae. Ecology80, 1267–1277 (1999).
Lagrue, C. & Poulin, R. Bottom–up regulation of parasite population densities in freshwater ecosystems. Oikos124, 1639–1647 (2015).
Lima, D. P. Jr, Giacomini, H. C., Takemoto, R. M., Agostinho, A. A. & Bini, L. M. Patterns of interactions of a large fish–parasite network in a tropical floodplain. J. Anim. Ecol.81, 905–913 (2012). PubMed
Vilà, M. et al. Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol. Lett.14, 702–708 (2011). PubMed
Westfall, A. K. et al. Host-specific phenotypic variation of a parasite co-introduced with invasive Burmese pythons. PLOS ONE. 14, e0209252 (2019). PubMed PMC
Santicchia, F. et al. Spillover of an alien parasite reduces expression of costly behaviour in native host species. J. Anim. Ecol.89, 1559–1569 (2020). PubMed
Gagne, R. B. et al. Spread of an introduced parasite across the Hawaiian Archipelago independent of its introduced host. Freshw. Biol.60, 311–322 (2015).
Ondračková, M. et al. Non-native gobies facilitate the transmission of Bucephalus polymorphus (Trematoda). Parasites Vectors. 8, 382 (2015). PubMed PMC
Esposito, A., Foata, J. & Quilichini, Y. Parasitic helminths and freshwater fish introduction in Europe: a systematic review of dynamic interactions. Fishes8, 450 (2023).
Schatz, A. M. & Park, A. W. Host and parasite traits predict cross-species parasite acquisition by introduced mammals. Philos. Trans. R Soc. B-Biol Sci.288, 20210341 (2021). PubMed PMC
Smith, C., Reichard, M., Jurajda, P. & Przybylski, M. The reproductive ecology of the European bitterling (Rhodeus sericeus). J. Zool.262, 107–124 (2004).
Labecka, A. M. & Reichard, M. The reproductive costs of bitterling fish and zebra mussel parasitism to a unionid mussel. Aquaculture595, 741515 (2025).
Soler, J., Wantzen, K. M. & Araujo, R. Rhodeus amarus (Bloch, 1782): a new potential threat for Margaritifera auricularia (Spengler, 1793) (Unionoida, Margaritiferidae). Freshw. Sci.38, 406–411 (2019).
Halabowski, D. et al. The depressed river mussel Pseudanodonta complanata as an occasional host for the European bitterling Rhodeus amarus. Knowl. Manag Aquat. Ecosyst.310.1051/kmae/2023025 (2024).
Holčík, J. & de Wit, J. J. D. The taxonomic characteristics of hybrid Rhodeus. Copeia1962, 777–788 (1962).
Sousa, R. et al. Microcondylaea bonellii as a new host for the European bitterling Rhodeus amarus. Knowl. Manag Aquat. Ecosyst.410.1051/kmae/2019047 (2020).
Rouchet, R. et al. Avoidance of host resistance in the oviposition-site preferences of rose bitterling. Evol Ecol31, 769–783 (2017).
Reichard, M. et al. Population-specific responses to an invasive species. Philos. Trans. R Soc. B-Biol Sci.282, 20151063 (2015). PubMed PMC
Smith, C., Rippon, K., Douglas, A. & Jurajda, P. A proximate cue for oviposition site choice in the bitterling (Rhodeus sericeus). Freshw. Biol.46, 903–911 (2001).
GiOŚ. Dane archiwalne i bieżące z monitoringu wód powierzchniowych - Portal jakości wód powierzchniowych. (2024). https://wody.gios.gov.pl/pjwp/publication/367
Mehler, K. et al. Recent and future distribution of the alien Chinese pond mussel Sinanodonta woodiana (Lea, 1834) on the European continent. Aquat. Invasions. 19, 51–72 (2024).
R Development Core Team. R: A language and Environment for Statistical Computing. Vienna, (2020).
Brooks, M. GlmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J.9, 378 (2017).
Hartig, F. & DHARMa Residual Diagnostics for Hierarchical (Multi-Level / Mixed) Regression Models. 0.4.7 (2021). 10.32614/CRAN.package.DHARMa
Wickham, H., Chang, W. & Wickham, M. Package ‘ggplot2’. Create elegant data visualisations using the grammar of graphics. (2016).
Zuur, A. F. & Ieno, E. N. A protocol for conducting and presenting results of regression-type analyses. Methods Ecol. Evol.7, 636–645 (2016).
Reichard, M., Przybylski, M., Kaniewska, P., Liu, H. & Smith, C. A possible evolutionary lag in the relationship between freshwater mussels and European bitterling. J. Fish. Biol.70, 709–725 (2007).
Reichard, M., Vrtílek, M., Douda, K. & Smith, C. An invasive species reverses the roles in a host–parasite relationship between bitterling fish and unionid mussels. Biol. Lett.8, 601–604 (2012). PubMed PMC
Marčić, Z. et al. Is bitterling (Rhodeus amarus (Bloch, 1782)) threatened by the invasive unionid species Sinanodonta woodiana (Lea, 1834)? Biol. Invasions. 26, 3417–3431 (2024).
Smith, C., Reynolds, J. D., Sutherland, W. J. & Jurajda, P. Adaptive host choice and avoidance of superparasitism in the spawning decisions of bitterling (Rhodeus sericeus). Behav. Ecol. Sociobiol.48, 29–35 (2000).
Reynolds, J. D., Debuse, V. J. & Aldridge, D. C. Host specialisation in an unusual symbiosis: European bitterlings spawning in freshwater mussels. Oikos78, 539–545 (1997).
Reichard, M., Bryja, J., Polačik, M. & Smith, C. No evidence for host specialization or host-race formation in the European bitterling (Rhodeus amarus), a fish that parasitizes freshwater mussels. Mol. Ecol.20, 3631–3643 (2011). PubMed
Phillips, A., Reichard, M. & Smith, C. Sex differences in the responses to oviposition site cues by a fish revealed by tests with an artificial host. Anim. Behav.126, 187–194 (2017).
Kryger, J. & Riisgård, H. U. Filtration rate capacities in 6 species of European freshwater bivalves. Oecologia77, 34–38 (1988). PubMed
Mills, S. C. & Reynolds, J. D. Host species preferences by bitterling, Rhodeus sericeus, spawning in freshwater mussels and consequences for offspring survival. Anim. Behav.63, 1029–1036 (2002).
Smith, C., Reichard, M. & Jurajda, P. Assessment of sperm competition by European bitterling, Rhodeus sericeus. Behav. Ecol. Sociobiol.53, 206–213 (2003).
Brian, J. I. & Aldridge, D. C. Abundance data applied to a novel model invertebrate host shed new light on parasite community assembly in nature. J. Anim. Ecol.90, 1096–1108 (2021). PubMed
Lundquist, S. P., Worthington, T. A. & Aldridge, D. C. Freshwater mussels as a tool for reconstructing climate history. Ecol. Indic.101, 11–21 (2019).
Watters, G. A synthesis and review of the expanding range of the Asian freshwater mussel Anodonta woodiana (Lea, 1834) (Bivalvia: Unionidae). Veliger40, 152–156 (1997).
Kraszewski, A. & Zdanowski, B. The distribution and abundance of the Chinese mussel Anodonta woodiana (Lea, 1834) in the heated Konin lakes. Fish. Aquat. Life9, 253–265 (2001).
Konečný, A. et al. Modelling the invasion history of Sinanodonta woodiana in Europe: tracking the routes of a sedentary aquatic invader with mobile parasitic larvae. Evol. Appl.11, 1975–1989 (2018). PubMed PMC
Lajtner, J. & Crncan, P. Distribution of the invasive bivalve Sinanodonta woodiana (Lea, 1834) in Croatia. Aquat. Invasions. 6, S119–S124 (2011).
Chang, C. H. et al. Phylogenetic relationships of Acheilognathidae (Cypriniformes: Cyprinoidea) as revealed from evidence of both nuclear and mitochondrial gene sequence variation: evidence for necessary taxonomic revision in the family and the identification of cryptic species. Mol. Phylogenet Evol.81, 182–194 (2014). PubMed
Shine, R. The ecological impact of invasive cane toads (Bufo marinus) in Australia. Q. Rev. Biol.85, 253–291 (2010). PubMed
Doody, J. S., Castellano, C. M., Rhind, D. & Green, B. Indirect facilitation of a native mesopredator by an invasive species: are cane toads re-shaping tropical riparian communities? Biol. Invasions. 15, 559–568 (2013).
Phillips, B. L. & Shine, R. An invasive species induces rapid adaptive change in a native predator: Cane Toads and black snakes in Australia. Proc. R. Soc. B. Biol. Sci.273, 1545–1550 (2006). PubMed PMC
Melotto, A., Ficetola, G. F., Alari, E., Romagnoli, S. & Manenti, R. Visual recognition and coevolutionary history drive responses of amphibians to an invasive predator. Behav. Ecol.32, 1352–1362 (2021).
Brian, J. I. & Aldridge, D. C. Endosymbionts: an overlooked threat in the conservation of freshwater mussels? Biol. Conserv.237, 155–165 (2019).
Hopkins, S. R., Ocampo, J. M., Wojdak, J. M. & Belden, L. K. Host community composition and defensive symbionts determine trematode parasite abundance in host communities. Ecosphere7, e01278 (2016).
Fisher, G., Dimock, R. & Kuhn, R. The symbiotic water mite Unionicola formosa (Acari: Unionicolidae) ingests mucus and tissue of its molluscan host. J. Parasitol.86, 1254–1258 (2001). PubMed
Gangloff, M. M., Lenertz, K. K. & Feminella, J. W. Parasitic mite and trematode abundance are associated with reduced reproductive output and physiological condition of freshwater mussels. Hydrobiologia610, 25–31 (2008).
Lewisch, E. et al. Parasites and their impact on thick-shelled river mussels Unio crassus from two populations in Luxembourg. Dis. Aquat. Org.153, 31–43 (2023). PubMed
Mills, S. C. & Reynolds, J. D. Mussel ventilation rates as a proximate cue for host selection by bitterling, Rhodeus sericeus. Oecologia131, 473–478 (2002). PubMed
Jokela, J., Uotila, L. & Taskinen, J. Effect of the castrating trematode parasite Rhipidocotyle fennica on energy allocation of fresh-water clam Anodonta piscinalis. Funct. Ecol.7, 332–338 (1993).
Walker, K. F. Reproductive phenology of river and lake populations of freshwater mussels (Unionida: Hyriidae) in the river Murray. Molluscan Res.37, 31–44 (2017).
Taskinen, J. & Valtonen, E. T. Age-, size-, and sex-specific infection of Anodonta piscinalis (Bivalvia: Unionidae) with Rhipidocotyle Fennica (Digenea: Bucephalidae) and its influence on host reproduction. Can. J. Zool.73, 887–897 (1995).
Wiśniewski, K. et al. Native and non-native Unionids respond differently to the presence of fouling dreissenid mussels. NeoBiota96, 1–18 (2024).
Bartáková, V. & Reichard, M. No effect of recent sympatry with invasive zebra mussel on the oviposition decisions and reproductive success of the bitterling fish, a brood parasite of unionid mussels. Hydrobiologia794, 153–166 (2017).
Ferreira-Rodríguez, N. et al. Research priorities for freshwater mussel conservation assessment. Biol. Conserv.231, 77–87 (2019).
Lopes-Lima, M. et al. Conservation status of freshwater mussels in Europe: state of the Art and future challenges. Biol. Rev.92, 572–607 (2017). PubMed
Lopes-Lima, M. et al. Conservation of freshwater bivalves at the global scale: diversity, threats and research needs. Hydrobiologia810, 1–14 (2018).
Sousa, R. et al. A roadmap for the conservation of freshwater mussels in Europe. Conserv. Biol.37, e13994 (2023). PubMed
Labecka, A. M. & Domagala, J. Continuous reproduction of Sinanodonta woodiana (Lea, 1824) females: an invasive mussel species in a female-biased population. Hydrobiologia810, 57–76 (2018).
Labecka, A. M. & Domagala, J. Two pathways for spermatogenesis in Sinanodonta woodiana (Lea, 1834) (Bivalvia: Unionidae). J. Molluscan Stud.85, 300–310 (2019).
Douda, K. et al. Review of the globally invasive freshwater mussels in the genus Sinanodonta Modell, 1945. Hydrobiologia 852, 1243–1273 (2024).
Douda, K., Vrtílek, M., Slavík, O. & Reichard, M. The role of host specificity in explaining the invasion success of the freshwater mussel Anodonta woodiana in Europe. Biol. Invasions. 14, 127–137 (2012).
Bielen, A. et al. Differences in tolerance to anthropogenic stress between invasive and native bivalves. Sci. Total Environ.543, 449–459 (2016). PubMed
Zieritz, A. et al. Towards the conservation of Borneo’s freshwater mussels: rediscovery of the endemic Ctenodesma borneensis and first record of the non-native Sinanodonta lauta. Biodivers. Conserv.29, 2235–2253 (2020).
Urbańska, M., Kamocki, A., Kirschenstein, M. & Ożgo, M. The Chinese pond mussel Sinanodonta woodiana demographically outperforms European native mussels. Sci. Rep.11, 17058 (2021). PubMed PMC
Donrovich, S. W. et al. Invasive Chinese pond mussel Sinanodonta woodiana threatens native mussel reproduction by inducing cross-resistance of host fish. Aquat. Conserv. -Mar Freshw. Ecosyst.27, 1325–1333 (2017).
Van Damme, D., Bogutskaya, N., Hoffmann, R. C. & Smith, C. The introduction of the European bitterling (Rhodeus amarus) to West and Central Europe. Fish Fish.8, 79–106 (2007).