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Environmental and spatial determinants of parasite communities in invasive and native freshwater fishes

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Abstract

Understanding why certain host species harbor more parasites is an important question in parasite and fish ecology. Parasite infection among sympatric species may integrate various processes affecting parasite assembly, including the species-specific ecology and the success of invaders. We focused on spatial, environmental, and host-related determinants of parasite assembly in three riverine fish species: the native three-spined stickleback and stone loach, and the invasive topmouth gudgeon. Parasite community structure differed significantly between the three host species. Three-spined stickleback harbored the most ectoparasites. Host density and nutrients were the strongest predictors of its parasite communities. Topmouth gudgeon harbored the lowest number of parasites, both in terms of abundance and species richness. None of the parasites identified originated from its expanded range, suggesting that enemy release occurred during invasion. Temperature and host density predicted parasite assemblages of topmouth gudgeon. Stone loach hosted the most endoparasites, likely resulting from its varied diet, benthic lifestyle, and larger size. Additionally, host size and condition were positively correlated with parasite infection, which was similar among the three host species. The results suggest that host-related factors have a similar effect among host species, while the importance of environmental and spatial factors differs according to host ecology.

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References

  • Ahne, W. & I. Thomsen, 1986. Isolation of pike fry rhabdovirus from Pseudorasbora parva (Temminck & Schlegel). Journal of Fish Diseases 9: 555–556.

    Google Scholar 

  • Andreou, D. & R. E. Gozlan, 2016. Associated disease risk from the introduced generalist pathogen Sphaerothecum destruens: management and policy implications. Parasitology 143: 1204–1210.

    PubMed  Google Scholar 

  • Andreou, D., R. E. Gozlan, D. Stone, P. Martin, K. Bateman & S. W. Feist, 2011. Sphaerothecum destruens pathology in cyprinids. Diseases of Aquatic Organisms 95: 145–151.

    CAS  PubMed  Google Scholar 

  • Arneberg, P., A. Skor**, B. Grenfell & A. F. Read, 1998. Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society B: Biological Sciences 265: 1283–1289.

    PubMed Central  Google Scholar 

  • Baia, R. R. J., A. C. Florentino, L. M. A. Silva & M. Tavares-Dias, 2018. Patterns of the parasite communities in a fish assemblage of a river in the Brazilian Amazon region. Acta Parasitologica 63: 304–316.

    PubMed  Google Scholar 

  • Barber, I. & J. P. Scharsack, 2010. The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 137: 411–424.

    CAS  PubMed  Google Scholar 

  • Barber, I., 2013. Sticklebacks as model hosts in ecological and evolutionary parasitology. Trends in Parasitology 29: 556–566.

    PubMed  Google Scholar 

  • Barger, M. A. & G. W. Esch, 2001. Downstream changes in the composition of the parasite community of fishes in an Appalachian stream. The Journal of Parasitology 87: 250–255.

    CAS  PubMed  Google Scholar 

  • Barluenga, M. & A. Meyer, 2005. Old fish in a young lake: stone loach (Pisces: Barbatula barbatula) populations in Lake Constance are genetically isolated by distance. Molecular Ecology 14: 1229–1239.

    CAS  PubMed  Google Scholar 

  • Barnosky, A. D., N. Matzke, S. Tomiya, G. O. U. Wogan, B. Swartz, T. B. Quental, C. Marshall, J. L. McGuire, E. L. Lindsey, K. C. Maguire, B. Mersey & E. A. Ferrer, 2011. Has the Earth’s sixth mass extinction already arrived? Nature 471: 51–57.

    CAS  PubMed  Google Scholar 

  • Behnke, J. M., 2008. Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions …. or pure randomness? Parasitology 135: 751–766.

    CAS  PubMed  Google Scholar 

  • Benesh, D. P., J. C. Chubb & G. A. Parker, 2014. The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths. Proceedings of the Royal Society B: Biological Sciences 281: 20141462.

    PubMed  PubMed Central  Google Scholar 

  • Beyer, K., G. H. Copp & R. E. Gozlan, 2007. Microhabitat use and interspecific associations of introduced topmouth gudgeon Pseudorasbora parva and native fishes in a small stream. Journal of Fish Biology 71: 224–238.

    Google Scholar 

  • Bize, P., C. Jeanneret, A. Klopfenstein & A. Roulin, 2008. What makes a host profitable? Parasites balance host nutritive resources against immunity. American Naturalist 171: 107–118.

    Google Scholar 

  • Blanar, C. A., D. J. Marcogliese & C. M. Couillard, 2011. Natural and anthropogenic factors shape metazoan parasite community structure in mummichog (Fundulus heteroclitus) from two estuaries in New Brunswick, Canada. Folia Parasitologica 58(3): 240.

  • Blanchet, F. G., P. Legendre & D. Borcard, 2008. Forward selection of explanatory variables. Ecology 89: 2623–2632.

    PubMed  Google Scholar 

  • Blasco-Costa, I., A. V. Koehler, A. Martin & R. Poulin, 2013. Upstream-downstream gradient in infection levels by fish parasites: A common river pattern? Parasitology 140(2): 266–274.

  • Borcard, D., F. Gillet & P. Legendre, 2011. Numerical Ecology with R, Springer:

    Google Scholar 

  • Borer, E. T., C. E. Mitchell, A. G. Power & E. W. Seabloom, 2009. Consumers indirectly increase infection risk in grassland food webs. Proceedings of the National Academy of Sciences of the United States of America 106: 503–506.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brouat, C., M. Kane, M. Diouf, K. Bâ, R. Sall-Dramé & J. M. Duplantier, 2007. Host ecology and variation in helminth community structure in Mastomys rodents from Senegal. Parasitology 134: 437–450.

    CAS  PubMed  Google Scholar 

  • Buchmann, K. & T. Lindenstrøm, 2002. Interactions between monogenean parasites and their fish hosts. International Journal for Parasitology 32: 309–319.

    PubMed  Google Scholar 

  • Budria, A., 2017. Beyond troubled waters: the influence of eutrophication on host–parasite interactions. Functional Ecology 31: 1348–1358.

    Google Scholar 

  • Budria, A. & U. Candolin, 2014. How does human-induced environmental change influence host−parasite interactions? Parasitology 141: 462–474.

    PubMed  Google Scholar 

  • Carrassón, M., S. Dallarés, J. E. Cartes, M. Constenla, A. Pérez-del-Olmo, L. Zucca & A. Kostadinova, 2019. Drivers of parasite community structure in fishes of the continental shelf of the Western Mediterranean: the importance of host phylogeny and autecological traits. International Journal for Parasitology 49: 669–683.

    PubMed  Google Scholar 

  • Colautti, R. I., A. Ricciardi, I. A. Grigorovich & H. J. MacIsaac, 2004. Is invasion success explained by the enemy release hypothesis? Ecology Letters 7: 721–733.

    Google Scholar 

  • Craft, M. E., P. L. Hawthorne, C. Packer & A. P. Dobson, 2008. Dynamics of a multihost pathogen in a carnivore community. Journal of Animal Ecology 77: 1257–1264.

    CAS  Google Scholar 

  • Cronin, J. P., M. E. Welsh, M. G. Dekkers, S. T. Abercrombie & C. E. Mitchell, 2010. Host physiological phenotype explains pathogen reservoir potential. Ecology Letters 13: 1221–1232.

    PubMed  Google Scholar 

  • Czeczuga, B., B. Kiziewicz & Z. Danilkiewicz, 2002. Zoosporic fungi growing on the specimens of certain fish species recently introduced to Polish waters. Acta Ichthyologica Et Piscatoria 2: 117–125.

    Google Scholar 

  • Dallas, T. & S. J. Presley, 2014. Relative importance of host environment, transmission potential and host phylogeny to the structure of parasite metacommunities. Oikos 123: 866–874.

    Google Scholar 

  • de Montaudouin, X. & L. Lanceleur, 2011. Distribution of parasites in their second intermediate host, the cockle Cerastoderma edule: community heterogeneity and spatial scale. Marine Ecology Progress Series 428: 187–199.

    Google Scholar 

  • Declerck, S., G. Louette, T. De Bie & L. De Meester, 2002. Patterns of diet overlap between populations of non-indigenous and native fishes in shallow ponds. Journal of Fish Biology 61: 1182–1197.

    Google Scholar 

  • Deflem, I. S., E. Bennetsen, Ø. H. Opedal, F. C. Calboli, O. Ovaskainen, G. Van Thuyne, et al., 2021. Predicting fish community responses to environmental policy targets. Biodiversity and Conservation 30: 1457–1478.

    Google Scholar 

  • Dobson, A., K. D. Lafferty, A. M. Kuris, R. F. Hechinger & W. Jetz, 2008. Homage to Linnaeus: how many parasites? How many hosts? Proceedings of the National Academy of Sciences of the United States of America 105: 11482–11489.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dormann, C. F., J. Elith, S. Bacher, C. Buchmann, G. Carl, G. Carré, J. R. G. Marquéz, B. Gruber, B. Lafourcade, P. J. Leitão, T. Münkemüller, C. Mcclean, P. E. Osborne, B. Reineking, B. Schröder, A. K. Skidmore, D. Zurell & S. Lautenbach, 2013. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36: 27–46.

    Google Scholar 

  • Fellis, K. J. & G. W. Esch, 2005. Variation in life cycle affects the distance decay of similarity among bluegill sunfish parasite communities. Journal of Parasitology 91: 1484–1486.

    Google Scholar 

  • Fourtune, L., I. Paz-Vinas, G. Loot, J. G. Prunier & S. Blanchet, 2016. Lessons from the fish: a multi-species analysis reveals common processes underlying similar species-genetic diversity correlations. Freshwater Biology 61: 1830–1845.

    Google Scholar 

  • Froese, R., 2006. Cube law, condition factor and weight-length relationships: history, meta-analysis and recommendations. Journal of Applied Ichthyology 22: 241–253.

    Google Scholar 

  • Galli, P., G. Strona, F. Benzoni, G. Crosa & F. Stefani, 2007. Monogenoids from freshwater fish in Italy, with comments on alien species. Comparative Parasitology 74: 264–272.

    Google Scholar 

  • Goater, C. P., R. E. Baldwin & G. J. Scrimgeour, 2005. Physico-chemical determinants of helminth component community structure in whitefish (Coregonus clupeaformes) from adjacent lakes in Northern Alberta, Canada. Parasitology 131: 713–722.

    CAS  PubMed  Google Scholar 

  • Goedknegt, M. A., M. E. Feis, K. M. Wegner, P. C. Luttikhuizen, C. Buschbaum, K. C. Camphuysen, J. van der Meer & D. W. Thieltges, 2016. Parasites and marine invasions: ecological and evolutionary perspectives. Journal of Sea Research 113: 11–27.

  • Gómez, A. & E. Nichols, 2013. Neglected wild life: parasitic biodiversity as a conservation target. International Journal for Parasitology: Parasites and Wildlife 2: 222–227.

    PubMed  PubMed Central  Google Scholar 

  • Gozlan, R. E., 2002. Occurrence of the Asiatic cyprinid Pseudorasbora parva in England. Journal of Fish Biology 61: 298–300.

    Google Scholar 

  • Gozlan, R. E., D. Andreou, T. Asaeda, K. Beyer, R. Bouhadad, D. Burnard, N. Caiola, P. Cakic, V. Djikanovic, H. R. Esmaeili, I. Falka, D. Golicher, A. Harka, G. Jeney, V. Kováč, J. Musil, A. Nocita, M. Povz, N. Poulet, et al., 2010. Pan-continental invasion of Pseudorasbora parva: towards a better understanding of freshwater fish invasions. Fish and Fisheries 11: 315–340.

    Google Scholar 

  • Gozlan, R. E., E. J. Peeler, M. Longshaw, S. St-Hilaire & S. W. Feist, 2006. Effect of microbial pathogens on the diversity of aquatic populations, notably in Europe. Microbes and Infection 8: 1358–1364.

    PubMed  Google Scholar 

  • Gozlan, R. E., S. S. Hilaire, S. W. Feist, P. Martin & M. L. Kent, 2005. Biodiversity: disease threat to European fish. Nature 435: 1046–1046.

    CAS  PubMed  Google Scholar 

  • Gozlan, R. E., C. M. Whipps, D. Andreou & K. D. Arkush, 2009. Identification of a rosette—like agent as Sphaerothecum destruens, a multi-host fish pathogen. International Journal for Parasitology 39: 1055–1058.

    CAS  PubMed  Google Scholar 

  • Grutter, A. S. & R. Poulin, 1998. Intraspecific and interspecific relationships between host size and the abundance of parasitic larval gnathiid isopods on coral reef fishes. Marine Ecology Progress Series 164: 263–271.

    Google Scholar 

  • Hablützel, P. I., A. F. Grégoir, M. P. M. Vanhove, F. A. M. Volckaert & J. A. M. Raeymaekers, 2016. Weak link between dispersal and parasite community differentiation or immunogenetic divergence in two sympatric cichlid fishes. Molecular Ecology 25: 5451–5466.

    PubMed  Google Scholar 

  • Hablützel, P. I., M. P. Vanhove, P. Deschepper, A. F. Grégoir, A. K. Roose, F. A. Volckaert & J. A. Raeymaekers, 2017. Parasite escape through trophic specialization in a species flock. Journal of Evolutionary Biology 30: 1437–1445.

    PubMed  Google Scholar 

  • Hansen, E. & R. Poulin, 2006. Spatial covariation between infection levels and intermediate host densities in two trematode species. Journal of Helminthology 80: 255–259.

    CAS  PubMed  Google Scholar 

  • Hartvigsen, R. & O. Halvorsen, 1994. Spatial patterns in the abundance and distribution of parasites of freshwater fish. Parasitology Today 10: 28–31.

    CAS  PubMed  Google Scholar 

  • Jarkovský, J., B. Koubková, T. Scholz, M. Prokeš & V. Baruš, 2004. Seasonal dynamics of Proteocephalus sagittus in the stone loach Barbatula barbatula from the Haná River, Czech Republic. Journal of Helminthology 78: 225–229.

    PubMed  Google Scholar 

  • Kakalova, E. & L. Shonia, 2008. The results of ecological-parasitological study of Pseudorasbora parva populated in Kumisi reservoir and Basaleti lake. Proceedings of the Institute of Zoology 23: 41–42.

    Google Scholar 

  • Kalbe, M., K. M. Wegner & T. B. H. Reusch, 2002. Dispersion patterns of parasites in 0+ year three−spined sticklebacks: a cross population comparison. Journal of Fish Biology 60(6): 1529–1542.

    Google Scholar 

  • Kangur, A. & P. Kangur, 1998. Diet composition and size−related changes in the feeding of pikeperch, Stizostedion lucioperca (Percidae) and pike, Esox lucius (Esocidae) in the lake Peipsi (Estonia). Italian Journal of Zoology 65(S1): 255–259.

    Google Scholar 

  • Kapusta, A., E. Bogacka-Kapusta & B. Czarnecki, 2008. The significance of stone moroko, Pseudorasbora parva (Temminck and Schlegel), in the small-sized fish assemblages in the littoral zone of the heated lake Licheńskie. Fisheries and Aquatic Life 16: 49–62.

    Google Scholar 

  • Karvonen, A., B. K. Kristjánsson, S. Skúlason, M. Lanki, C. Rellstab & J. Jokela, 2013. Water temperature, not fish morph, determines parasite infections of sympatric Icelandic threespine sticklebacks (Gasterosteus aculeatus). Ecology and Evolution 3: 1507–1517.

    PubMed  PubMed Central  Google Scholar 

  • Kelly, D. W., R. A. Paterson, C. R. Townsend, R. Poulin & D. M. Tompkins, 2009. Parasite spillback: a neglected concept in invasion ecology? Ecology 90: 2047–2056.

    CAS  PubMed  Google Scholar 

  • Keskinen, T. & T. J. Marjomäki, 2004. Diet and prey size spectrum of pikeperch in lakes in central Finland. Journal of Fish Biology 65: 1147–1153.

    Google Scholar 

  • Kilpatrick, A. M., P. Daszak, M. J. Jones, P. P. Marra & L. D. Kramer, 2006. Host heterogeneity dominates West Nile virus transmission. Proceedings of the Royal Society B: Biological Sciences 273: 2327–2333.

    PubMed  Google Scholar 

  • Krasnov, B. R., G. I. Shenbrot, S. G. Medvedev, V. S. Vatschenok & I. S. Khokhlova, 1997. Host-habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114: 159–173.

    PubMed  Google Scholar 

  • Landis, G. A. M., T. L. Mosley, W. R. Haag & J. A. Stoeckel, 2012. Effects of temperature and photoperiod on lure display and glochidial release in a freshwater mussel. Freshwater Science 31: 775–786.

    Google Scholar 

  • Lazzaro, B. P. & T. J. Little, 2009. Immunity in a variable world. Philosophical Transactions of the Royal Society B: Biological Sciences 364: 15–26.

    Google Scholar 

  • Lee, K. A., 2006. Linking immune defenses and life history at the levels of the individual and the species. Integrative and Comparative Biology 46: 1000–1015.

    CAS  PubMed  Google Scholar 

  • Legendre, P. & E. D. Gallagher, 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271–280.

    PubMed  Google Scholar 

  • Lima, D. P., H. C. Giacomini, R. M. Takemoto, A. A. Agostinho & L. M. Bini, 2012. Patterns of interactions of a large fish-parasite network in a tropical floodplain. Journal of Animal Ecology 81: 905–913.

    Google Scholar 

  • Locke, S. A., M. S. Levy, D. J. Marcogliese, S. Ackerman & J. D. Mclaughlin, 2012. The decay of parasite community similarity in ring-billed gulls Larus delawarensis and other hosts. Ecography 35: 530–538.

    Google Scholar 

  • Loot, G., Y. Reyjol, N. Poulet, A. Simkova, S. Blanchet & S. Lek, 2007. Effects of small weirs on fish parasite communities. Parasitology Research 101: 1265–1276.

    PubMed  Google Scholar 

  • Lugert, V., E. I. Meyer, J. Kurtz & J. P. Scharsack, 2017. Effects of an anthropogenic saltwater inlet on three-spined stickleback (Gasterosteus aculeatus) (Teleostei: Gasterosteidae) and their parasites in an inland brook. The European Zoological Journal 84: 444–456.

    Google Scholar 

  • Luque, J. L. & R. Poulin, 2008. Linking ecology with parasite diversity in Neotropical fishes. Journal of Fish Biology 72: 189–204.

    Google Scholar 

  • Marcogliese, D. J., 2002. Food webs and the transmission of parasites to marine fish. Parasitology 124: 83–99.

    Google Scholar 

  • Marques, J. F., M. J. Santos, C. M. Teixeira, M. I. Batista & H. N. Cabral, 2011. Host-parasite relationships in flatfish (Pleuronectiformes)—the relative importance of host biology, ecology and phylogeny. Parasitology 138: 107–121.

    CAS  PubMed  Google Scholar 

  • Mitchell, C. E., & A. O. Power, 2003. Release of invasive plants from fungal and viral pathogens. Nature 421(6923): 625–627.

  • Nekola, J. C. & P. S. White, 1999. The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26: 867–878.

    Google Scholar 

  • Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’hara, G. L. Simpson, P. Solymos, M. H. Stevens, H. Wagner & M. J. Oksanen, 2013. Package ‘vegan’. Community ecology package, version 2(9): 1–295.

  • Ondračková, M., I. Matějusová, A. Šimková & M. Gelnar, 2004. New reports of dactylogyridean species (Monogenea) for Central Europe. Helminthologia 41(3): 139–145.

  • Pariselle, A., W. A. Boeger, J. Snoeks, C. F. Bilong Bilong, S. Morand & M. P. M. Vanhove, 2011. The monogenean parasite fauna of Cichlids: a potential tool for host biogeography. International Journal of Evolutionary Biology 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  • Peeler, E. J., B. C. Oidtmann, P. J. Midtlyng, L. Miossec & R. E. Gozlan, 2011. Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions 13: 1291–1303.

    Google Scholar 

  • Perkins, S. L., A. S. Kerwin & A. D. Rothschild, 2009. Patterns of infection of the lizard malaria parasite, Plasmodium floridense, in invasive brown anoles (Anolis sagrei) in Southwestern Florida. Parasitology Research 104: 1191–1196.

    PubMed  Google Scholar 

  • Petkova, I., R. N. Abbey-Lee & H. Løvlie, 2018. Parasite infection and host personality: Glugea-infected three-spined sticklebacks are more social. Behavioral Ecology and Sociobiology 72: 1–9.

    Google Scholar 

  • Ponton, F., K. Wilson, S. C. Cotter, D. Raubenheimer & S. J. Simpson, 2011. Nutritional immunology: a multi-dimensional approach. PLoS Pathogens 7: e1002223.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Postel, S. & B. Richter, 2003. Rivers for life: managing water for people and nature, Island Press:

    Google Scholar 

  • Poulin, R., 2000. Variation in the intraspecific relationship between fish length and intensity of parasitic infection: Biological and statistical causes. Journal of Fish Biology 56: 123–137.

    Google Scholar 

  • Poulin, R., 2007. Are there general laws in parasite ecology? Parasitology 134(6): 763–776.

    CAS  PubMed  Google Scholar 

  • Poulin, R. & T. L. F. Leung, 2011. Body size, trophic level, and the use of fish as transmission routes by parasites. Oecologia 166: 731–738.

    CAS  PubMed  Google Scholar 

  • Poulin, R. & S. Morand, 2000a. The diversity of parasites. The Quarterly Review of Biology 75: 277–293.

    CAS  PubMed  Google Scholar 

  • Poulin, R., 2003. The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30: 1609–1615.

    Google Scholar 

  • Poulin, R., 2010. Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41: 151–186.

    Google Scholar 

  • Poulin, R., C. A. Blanar, D. W. Thieltges & D. J. Marcogliese, 2011. The biogeography of parasitism in sticklebacks: distance, habitat differences and the similarity in parasite occurrence and abundance. Ecography 34: 540–551.

    Google Scholar 

  • Poulin, R. & M. R. Forbes, 2012. Meta-analysis and research on host-parasite interactions: past and future. Evolutionary Ecology 26: 1169–1185.

    Google Scholar 

  • Poulin, R. & S. Morand, 2000b. Testes size, body size and male-male competition in acanthocephalan parasites. Journal of Zoology 250: 551–558.

    Google Scholar 

  • Prenter, J., C. MacNeil, J. T. A. Dick & A. M. Dunn, 2004. Roles of parasites in animal invasions. Trends in Ecology & Evolution 19: 385–390.

    Google Scholar 

  • Přikrylová, I., I. Matějusová, J. Jarkovský & M. Gelnar, 2008. Morphometric comparison of three members of the Gyrodactylus nemachili-like species group (Monogenea: Gyrodactylidae) on Barbatula barbatula L. in the Czech Republic, with a reinstatement of G. papernai Ergens & Bychowsky, 1967. Systematic Parasitology 69: 33–44.

    PubMed  Google Scholar 

  • R Core Team, 2020. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Raeymaekers, J. A. M., T. Huyse, H. Maelfait, B. Hellemans & F. A. M. Volckaert, 2008. Community structure, population structure and topographical specialisation of Gyrodactylus (Monogenea) ectoparasites living on sympatric stickleback species. Folia Parasitologica 55: 187–196.

    PubMed  Google Scholar 

  • Raeymaekers, J. A., M. Wegner, T. Huyse & F. A. Volckaert, 2011. Infection dynamics of the monogenean parasite Gyrodactylus gasterostei on sympatric and allopatric populations of the three-spined stickleback Gasterosteus aculeatus. Folia parasitologica 58(1): 27–34.

  • Rahn, A. K., D. A. Hammer & T. C. M. Bakker, 2015. Experimental infection with the directly transmitted parasite Gyrodactylus influences shoaling behaviour in sticklebacks. Animal Behaviour 107: 253–261.

    Google Scholar 

  • Randhawa, H. S. & R. Poulin, 2010. Determinants of tapeworm species richness in elasmobranch fishes: untangling environmental and phylogenetic influences. Ecography 33: 866–877.

    Google Scholar 

  • Ripley, B., B. Venables, D. M. Bates, K. Hornik, A. Gebhardt, D. Firth & M. B. Ripley, 2013. Package ‘mass’. Cran r 538: 113–120.

  • Sana, S., E. A. Hardouin, R. E. Gozlan, D. Ercan, A. S. Tarkan, T. Zhang & D. Andreou, 2017. Origin and invasion of the emerging infectious pathogen Sphaerothecum destruens: origin of the emerging infectious pathogen. Emerging Microbes & Infections 6: 1–8.

    Google Scholar 

  • Sanchez-Thirion, K., M. Danger, A. Bec, E. Billoir, S. Labaude, T. Rigaud, J. N. Beisel & V. Felten, 2019. High food quality increases infection of Gammarus pulex (Crustacea: Amphipoda) by the acanthocephalan parasite Pomphorhynchus laevis. International Journal for Parasitology, 49: 805−817

  • Scholz, T., A. Škeříková, V. Hanzelová, B. Koubková & V. Baruš, 2003. Resurrection of Proteocephalus sagittus (Grimm, 1872) (Cestoda: Proteocephalidea) based on morphological and molecular data. Systematic Parasitology 56(3): 173–181.

  • Sheath, D. J., C. F. Williams, A. J. Reading & R. J. Britton, 2015. Parasites of non-native freshwater fishes introduced into England and Wales suggest enemy release and parasite acquisition. Biological Invasions 17: 2235–2246.

    Google Scholar 

  • Shershneva, A. V. & A. E. Zhokhov, 2013. Parasites of stone loach Barbatula barbatula (L., 1758) (Balitoridae) in small rivers of the upper and Middle Volga Basin. Inland Water Biology 6: 236–245.

    Google Scholar 

  • Šimková, A., J. Jarkovský, B. Koubková, V. Baruš & M. Prokeš, 2005. Associations between fish reproductive cycle and the dynamics of metazoan parasite infection. Parasitology Research 95: 65–72.

    PubMed  Google Scholar 

  • Soininen, J., R. McDonald & H. Hillebrand, 2007. The distance decay of similarity in ecological communities. Ecography 30: 3–12.

    Google Scholar 

  • Spikmans, F., P. Lemmers & H. J. M. op den Camp, E. van Haren, F. Kappen, A. Blaakmeer, G. van der Velde, F. van Langevelde, R. S. E. W. Leuven & T. A. van Alen, 2020. Impact of the invasive alien topmouth gudgeon (Pseudorasbora parva) and its associated parasite Sphaerothecum destruens on native fish species. Biological Invasions 22: 587–601.

    Google Scholar 

  • Strayer, D. L. & D. Dudgeon, 2010. Freshwater biodiversity conservation: recent progress and future challenges. Journal of the North American Benthological Society 29: 344–358.

    Google Scholar 

  • Studer, A., D. W. Thieltges & R. Poulin, 2010. Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Marine Ecology Progress Series 415: 11–22.

    Google Scholar 

  • Székely, C., A. Palstra, K. Molnár & G. van den Thillart, 2009. Impact of the swim-bladder parasite on the health and performance of European eels. In Spawning Migration of the European Eel. Springer, Dordrecht: 201−226

  • Takemoto, R. M., G. C. Pavanelli, M. A. P. Lizama, J. L. Luque & R. Poulin, 2005. Host population density as the major determinant of endoparasite species richness in floodplain fishes of the upper Paraná River, Brazil. Journal of Helminthology 79: 75–84.

    CAS  PubMed  Google Scholar 

  • Telfer, S., K. J. Bown, R. Sekules, M. Begon, T. Hayden & R. Birtles, 2005. Disruption of a host-parasite system following the introduction of an exotic host species. Parasitology 130: 661–668.

    CAS  PubMed  Google Scholar 

  • Thieltges, D. W., B. L. Fredensborg & R. Poulin, 2009. Geographical variation in metacercarial infection levels in marine invertebrate hosts: parasite species character versus local factors. Marine Biology 156: 983–990.

    Google Scholar 

  • Torchin, M. E., K. D. Lafferty, A. P. Dobson, V. J. McKenzie & A. M. Kuris, 2003. Introduced species and their missing parasites. Nature 421: 628–630.

    CAS  PubMed  Google Scholar 

  • Ward, A. J. W., A. J. Duff, J. Krause & I. Barber, 2005. Shoaling behaviour of sticklebacks infected with the microsporidian parasite, Glugea anomala. Environmental Biology of Fishes 72: 155–160.

    Google Scholar 

  • Wheeler, A., 1992. Freshwater Fishes of Britain and Europe, Rainbow Books, London:

    Google Scholar 

  • Wootten, Z. I. R., 2013. Population biology of a cestode, Proteocephalus filicollis (Rudolphi) from Gasterosteus aculeatus L. in Scotland. Canadian Journal of Pure and Applied Sciences, 2475.

  • Zander, C. D., 2005. Four-year monitoring of parasite communities in gobiid fishes of the southwest Baltic: III. Parasite species diversity and applicability of monitoring. Parasitology Research 95: 136–144.

    PubMed  Google Scholar 

  • Zhokhov, A. E., A. V. Shershneva & M. N. Pugacheva, 2016. A checklist of protozoan and metazoan parasites of the stone loach Barbatula barbatula (Cypriniformes, Balitoridae). Parasitology 50, 1.

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Acknowledgements

The Research Foundation-Flanders (FWO) supported research with a PhD scholarship to ISD (1S48119N). We thank Sarah Maes, Tim Maes, and Ruben Schols for assistance with field sampling, and Paulien Philippe for help with parasite screening. We thank the reviewers for their thoughtful comments.

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Authors and Affiliations

  1. Laboratory of Biodiversity and Evolutionary Genomics, KU Leuven, 3000, Leuven, Belgium

    Io S. Deflem, Frederik Van Den Eeckhaut, Mikaël Vandevoorde, Federico C. F. Calboli, Joost A. M. Raeymaekers & Filip A. M. Volckaert

  2. Natural Resources Institute Finland (Luke), 31600, Jokioinen, Finland

    Federico C. F. Calboli

  3. Faculty of Biosciences and Aquaculture, Nord University, 8049, Bodø, Norway

    Joost A. M. Raeymaekers

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  1. Io S. Deflem
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Contributions

ISD and FAMV designed the study. ISD and FCFC collected the samples. MV, FVDE, and ISD performed the parasite screening. ISD and JAMR analyzed the data. ISD wrote the manuscript with input from FCFC, JAMR, and FAMV. All authors contributed to the writing and approved the final version for publication. The authors declare that they have no competing interests.

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Correspondence to Io S. Deflem.

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Deflem, I.S., Van Den Eeckhaut, F., Vandevoorde, M. et al. Environmental and spatial determinants of parasite communities in invasive and native freshwater fishes. Hydrobiologia 849, 913–928 (2022). https://doi.org/10.1007/s10750-021-04746-z

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