Parasites comprise a huge part of the biodiversity on earth. However, on a local scale, not much is known about their diversity and community structure. Here, we assess the diversity of larval trematode communities in an interconnected freshwater system of the River Ruhr in Germany and analyse how the parasites are spatially and temporally distributed in the ecosystem. A total of 5347 snail hosts belonging to six species revealed a highly diverse parasite fauna with 36 trematode species. More abundant snail species harboured more species-rich trematode faunas and communities, with the two dominant snail species, Radix auricularia and Gyraulus albus, accounting for almost 90% of the trematode diversity and harbouring spatially and temporally stable parasite communities. The results highlight the important role of stable keystone host populations for trematode transmission, structure and diversity. This local trematode diversity reveals information on definitive host occurrence and trophic interactions within ecosystems.

Department of Aquatic Ecology University of Duisburg Essen 45141 Essen Germany

Department of Biology Aquatic Biology Aarhus University 8000 Aarhus C Denmark

Department of Zoology University of Johannesburg Johannesburg South Africa

Institute of Biodiversity and Ecosystem Research Bulgarian Academy of Sciences 2 Gagarin Street 1113 Sofia Bulgaria

Institute of Parasitology Biology Centre Czech Academy of Sciences 37005 České Budějovice Czech Republic

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Poulin R. The functional importance of parasites in animal communities: many roles at many levels? Int. J. Parasitol. 1999;29:903–914. doi: 10.1016/S0020-7519(99)00045-4. PubMed DOI

Hudson PJ, Dobson AP, Lafferty KD. Is a healthy ecosystem one that is rich in parasites? Trends Ecol. Evol. 2006;21:381–385. doi: 10.1016/j.tree.2006.04.007. PubMed DOI

Lafferty, K. D. et al. Food webs and parasites in a salt marsh ecosystem. In: Collinge, S. & Ray, C. (Eds.), Disease ecology: Community Structure and Pathogen Dynamics (Oxford University Press, Oxford, 2006).

Thomas F, Poulin R, de Meeus T, Guegan J-F, Renaud F. Parasites and ecosystem engineering: what roles could they play? Oikos. 1999;84:167–171. doi: 10.2307/3546879. DOI

Frainer A, McKie BG, Amundsen P-A, Knudsen R, Lafferty KD. Parasitism and the biodiversity-functioning relationship. Trends Ecol. Evol. 2018;33:1–9. doi: 10.1016/j.tree.2018.01.011. PubMed DOI

Hudson PJ, Dobson AP, Newborn D. Prevention of population cycles by parasite removal. Science. 1998;282:2256–2258. doi: 10.1126/science.282.5397.2256. PubMed DOI

Lefèvre T, et al. The ecological significance of manipulative parasites. Trends Ecol. Evol. 2009;24:41–48. doi: 10.1016/j.tree.2008.08.007. PubMed DOI

Lafferty KD, Morris AK. Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology. 1996;77:1390–1397. doi: 10.2307/2265536. DOI

Moore, J. Parasites and the Behavior of Animals. (Oxford University Press, Oxford, 2002).

Mouritsen KN, Poulin R. Parasite-induced trophic facilitation exploited by a non-host predator: a manipulator’s nightmare. Int. J. Parasitol. 2003;33:1043–1050. doi: 10.1016/S0020-7519(03)00178-4. PubMed DOI

Poulin R. Parasite manipulation of host behavior: An update and frequently asked questions. Adv. Stud. Behav. 2010;41:151–186. doi: 10.1016/S0065-3454(10)41005-0. DOI

Lafferty KD, et al. Parasites in food webs: the ultimate missing links. Ecol. Lett. 2008;11:533–546. doi: 10.1111/j.1461-0248.2008.01174.x. PubMed DOI PMC

Thieltges DW, Engelsma MY, Wendling CC, Wegner KM. Parasites in the Wadden Sea food web. J. Sea Res. 2013;82:122–133. doi: 10.1016/j.seares.2012.06.002. DOI

Wood M. Parasites entangled in food webs. Trends Parasitol. 2007;23:8–10. doi: 10.1016/j.pt.2006.11.003. PubMed DOI

Kuris AM, et al. Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature. 2008;454:515–518. doi: 10.1038/nature06970. PubMed DOI

Preston DL, Orlofske SA, Lambden JP, Johnson PTJ. Biomass and productivity of trematode parasites in pond ecosystems. J. Anim. Ecol. 2013;82:509–517. doi: 10.1111/1365-2656.12030. PubMed DOI

Soldánová M, Selbach C, Sures B. The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLOS ONE. 2016;11:e0149678. doi: 10.1371/journal.pone.0149678. PubMed DOI PMC

Thieltges DW, et al. Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Mar. Ecol. Prog. Ser. 2008;372:147–155. doi: 10.3354/meps07703. DOI

Sures B. Accumulation of heavy metals by intestinal helminths in fish: an overview and perspective. Parasitology. 2003;126:53–60. doi: 10.1017/S003118200300372X. PubMed DOI

Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W. Homage to Linnaeus: How many parasites? How many hosts? Proc. Natl. Acad. Sci. 2008;105:11482–11489. doi: 10.1073/pnas.0803232105. PubMed DOI PMC

Lafferty KD. Environmental parasitology: What can parasites tell us about human impacts on the environment? Parasitol. Today. 1997;13:251–255. doi: 10.1016/S0169-4758(97)01072-7. PubMed DOI

Huspeni TC, Lafferty KD. Using larval trematodes that parasitize snails to evaluate a saltmarsh restoration project. Ecol. Appl. 2004;14:795–804. doi: 10.1890/01-5346. DOI

Vidal-Martínez VM, Pech D, Sures B, Purucker ST, Poulin R. Can parasites really reveal environmental impact? Trends Parasitol. 2010;26:44–51. doi: 10.1016/j.pt.2009.11.001. PubMed DOI

Shea J. The use of parasites as indicators of ecosystem health as compared to insects in freshwater lakes of the Inland Northwest. Ecol. Indic. 2012;13:184–188.

Nachev M, Sures B. Environmental parasitology: Parasites as accumulation bioindicators in the marine environment. J. Sea Res. 2016;113:45–50. doi: 10.1016/j.seares.2015.06.005. DOI

Poulin, R. & Morand, S. Parasite Biodiversity. (Smithsonian Books, Washington, DC, 2004).

Poulin R. Parasite biodiversity revisited: frontiers and constraints. Int. J. Parasitol. 2014;44:581–589. doi: 10.1016/j.ijpara.2014.02.003. PubMed DOI

Okamura B, Hartigan A, Naldoni J. Extensive uncharted biodiversity: The parasite dimension. Integr.Comp. Biol. 2018;58:1132–1145. PubMed

Jorge F, Poulin R. Poor geographical match between the distributions of host diversity and parasite discovery effort. Proc. R. Soc. B Biol. Sci. 2018;285:20180072. doi: 10.1098/rspb.2018.0072. PubMed DOI PMC

Harvell CD, et al. Climate warming and disease risks for terrestrial and marine biota. Science. 2002;296:2158–2162. doi: 10.1126/science.1063699. PubMed DOI

Altizer S, Ostfeld RS, Johnson PTJ, Kutz S, Harvell CD. Climate change and infectious diseases: From evidence to a predictive framework. Science. 2013;341:514–519. doi: 10.1126/science.1239401. PubMed DOI

Jones KE, et al. Global trends in emerging infectious diseases. Nature. 2008;451:990–993. doi: 10.1038/nature06536. PubMed DOI PMC

Esch GW. The transmission of digenetic trematodes: Style, elegance, complexity. Integr. Comp. Biol. 2002;42:304–312. doi: 10.1093/icb/42.2.304. PubMed DOI

Hechinger RF, Lafferty KD, Huspeni TC, Brooks AJ, Kuris AM. Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia. 2007;151:82–92. doi: 10.1007/s00442-006-0568-z. PubMed DOI

Soldánová M, Selbach C, Sures B, Kostadinova A, Perez-Del-Olmo A. Larval trematode communities in Radix auricularia and Lymnaea stagnalis in a reservoir system of the Ruhr River. Parasit Vectors. 2010;3:56. doi: 10.1186/1756-3305-3-56. PubMed DOI PMC

Schwelm J, Soldánová M, Vyhlídalová T, Sures B, Selbach C. Small but diverse: larval trematode communities in the small freshwater planorbids Gyraulus albus and Segmentina nitida (Gastropoda: Pulmonata) from the Ruhr River, Germany. Parasitol. Res. 2018;117:241–255. doi: 10.1007/s00436-017-5699-0. PubMed DOI

Georgieva S, et al. New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasit Vectors. 2013;6:64. doi: 10.1186/1756-3305-6-64. PubMed DOI PMC

Selbach C, et al. Morphological and molecular data for larval stages of four species of Petasiger Dietz, 1909 (Digenea: Echinostomatidae) with an updated key to the known cercariae from the Palaearctic. Syst. Parasitol. 2014;89:153–166. doi: 10.1007/s11230-014-9513-4. PubMed DOI

Selbach, C., Soldánová, M., Georgieva, S., Kostadinova, A. & Sures, B. Integrative taxonomic approach to the cryptic diversity of Diplostomum spp. in lymnaeid snails from Europe with a focus on the ‘Diplostomum mergi’ species complex. Parasit Vectors8, 300 (2015). PubMed PMC

Gordy MA, Kish L, Tarrabain M, Hanington PC. A comprehensive survey of larval digenean trematodes and their snail hosts in central Alberta, Canada. Parasitol. Res. 2016;115:3867–3880. doi: 10.1007/s00436-016-5152-9. PubMed DOI

Bargues MD, et al. European Lymnaeidae (Mollusca: Gastropoda), intermediate hosts of trematodiases, based on nuclear ribosomal DNA ITS-2 sequences. Infect. Genet. Evol. 2001;1:85–107. doi: 10.1016/S1567-1348(01)00019-3. PubMed DOI

Faltýnková A, Haas W. Larval trematodes in freshwater molluscs from the Elbe to Danube rivers (Southeast Germany): before and today. Parasitol. Res. 2006;99:572–582. doi: 10.1007/s00436-006-0197-9. PubMed DOI

Faltýnková A. Larval trematodes (Digenea) in molluscs from small water bodies near České Budějovice, Czech Republic. Acta Parasitol. 2005;50:49–55.

Żbikowska E. Digenea species in chosen populations of freshwater snails in northern and central part of Poland. Wiadomości Parazytol. 2007;53:301–308. PubMed

Adam ME, Lewis JW. The role of Lymnaea auricularia (Linnaeus) and Lymnaea peregra (Müller) (Gastropoda: Pulmonata) in the transmission of larval digeneans in the lower Thames valley. J. Mollus. Stud. 1993;59:1–6. doi: 10.1093/mollus/59.1.1. DOI

Faltýnková A, Sures B, Kostadinova A. Biodiversity of trematodes in their intermediate mollusc and fish hosts in the freshwater ecosystems of Europe. Syst. Parasitol. 2016;93:283–293. doi: 10.1007/s11230-016-9627-y. PubMed DOI

Fecchio A, et al. Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds. Mol. Ecol. 2019;28:2681–2693. doi: 10.1111/mec.15094. PubMed DOI

Glöer P. Die Süßwassergastropoden Nord- und Mitteleuropas. (ConchBooks, Hackenheim, 2002).

Kuris, A. M., Blaustein, A. R. & Alio, J. J. Hosts as islands. Am. Nat.116, 570–586 (1980).

Kamiya T, O’Dwyer K, Nakagawa S, Poulin R. Host diversity drives parasite diversity: meta-analytical insights into patterns and causal mechanisms. Ecography. 2014;37:689–697. doi: 10.1111/j.1600-0587.2013.00571.x. DOI

Poulin R, Mouritsen KN. Large-scale determinants of trematode infections in intertidal gastropods. Mar. Ecol. Prog. Ser. 2003;254:187–198. doi: 10.3354/meps254187. DOI

Combes, C. Parasitism: The ecology and evolution of intimate interactions. Interspecific interactions. (University of Chicago Press, Chicago, Illinois, 2001).

Marcogliese DJ. Parasites: Small players with crucial roles in the ecological theater. EcoHealth. 2004;1:151–164. doi: 10.1007/s10393-004-0028-3. DOI

Seppälä O, Karvonen A, Valtonen ET. Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke-fish interaction. Anim. Behav. 2004;68:257–263. doi: 10.1016/j.anbehav.2003.10.021. DOI

Vivas Muñoz JC, Staaks G, Knopf K. The eye fluke Tylodelphys clavata affects prey detection and intraspecific competition of European perch (Perca fluviatilis) Parasitol. Res. 2017;116:2561–2567. doi: 10.1007/s00436-017-5564-1. PubMed DOI

Padrós F, Knudsen R, Blasco-Costa I. Histopathological characterisation of retinal lesions associated to Diplostomum species (Platyhelminthes: Trematoda) infection in polymorphic Arctic charr Salvelinus alpinus. Int. J. Parasitol. Parasites Wildl. 2018;7:68–74. doi: 10.1016/j.ijppaw.2018.01.007. PubMed DOI PMC

Poulin, R. Evolutionary Ecology of Parasites. (Princeton University Press, Princeton, 2007).

Brown R, Soldánová M, Barrett J, Kostadinova A. Small-scale to large-scale and back: larval trematodes in Lymnaea stagnalis and Planorbarius corneus in Central Europe. Parasitol. Res. 2011;108:137–150. doi: 10.1007/s00436-010-2047-z. PubMed DOI

Soldánová M, Faltýnková A, Scholz T, Kostadinova A. Parasites in a man-made landscape: contrasting patterns of trematode flow in a fishpond area in Central Europe. Parasitology. 2011;138:789–807. doi: 10.1017/S0031182011000291. PubMed DOI

Lawton SP, et al. Unravelling the riddle of Radix: DNA barcoding for species identification of freshwater snail intermediate hosts of zoonotic digeneans and estimating their inter-population evolutionary relationships. Infect. Genet. Evol. 2015;35:63–74. doi: 10.1016/j.meegid.2015.07.021. PubMed DOI

Faltýnková A, Našincová V, Kablásková L. Larval trematodes (Digenea) of the great pond snail, Lymnaea stagnalis (L.), (Gastropoda, Pulmonata) in Central Europe: a survey of species and key to their identification. Parasite. 2007;14:39–51. doi: 10.1051/parasite/2007141039. PubMed DOI

Faltýnková A, Našincová V, Kablásková L. Larval trematodes (Digenea) of planorbid snails (Gastropoda: Pulmonata) in Central Europe: a survey of species and key to their identification. Syst. Parasitol. 2008;69:155–178. doi: 10.1007/s11230-007-9127-1. PubMed DOI

Niewiadomska K. Verification of the life-cycles of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae) Syst. Parasitol. 1986;8:23–31. doi: 10.1007/BF00010306. DOI

Niewiadomska K, Kiseliene V. Diplostomum cercariae (Digenea) in snails from Lithuania. II. Survey of species. Acta Parasitol. 1994;39:179–186.

Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 1997;83:575–83. doi: 10.2307/3284227. PubMed DOI

Clarke, K. R. & Gorley, R. N. PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, 192pp. (2006).

Esch GW, Curtis LA, Barger MA. A perspective on the ecology of trematode communities in snails. Parasitology. 2001;123:57–75. doi: 10.1017/S0031182001007697. PubMed DOI

Hugghins EJ. Life history of a strigeid trematode, Hysteromorpha triloba (Rudolphi, 1819) Lutz, 1931. II. Sporocyst through adult. T. Am. Micros. Soc. 1954;73:221. doi: 10.2307/3224061. DOI

Našincová V, Scholz T. The life cycle of Asymphylodora tincae (Modeer 1790) (Trematoda: Monorchiidae): a unique development in monorchiid trematodes. Parasitol. Res. 1994;80:192–197. doi: 10.1007/BF00932673. PubMed DOI

Dubois G. Synopsis des Strigeidae et des Diplostomatidae (Trematoda) Bull. Soc. Neuchl. Sci. Nat. 1968;10:1–258.

Taft Stephen J. Some Aspects of the Larval Development of Cyclocoelum obscurum (Trematoda: Cyclocoelidae) The Journal of Parasitology. 1973;59(1):90. doi: 10.2307/3278577. PubMed DOI

McLaughlin JD. Experimental studies on the life cycle of Cyclocoelum mutabile (Zeder) (Trematoda: Cyclocoelidae) Can. J. Zool. 1976;54:48–54. doi: 10.1139/z76-005. PubMed DOI

Tkach VV, Kudlai O, Kostadinova A. Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea) Int. J. Parasitol. 2016;46:171–185. doi: 10.1016/j.ijpara.2015.11.001. PubMed DOI

Lagrue C, Poulin R, Cohen JE. Parasitism alters three power laws of scaling in a metazoan community: Taylor’s law, density-mass allometry, and variance-mass allometry. Proc. Natl. Acad. Sci. 2015;112:1791–1796. doi: 10.1073/pnas.1422475112. PubMed DOI PMC

Richgels KLD, Hoverman JT, Johnson PTJ. Evaluating the role of regional and local processes in structuring a larval trematode metacommunity of Helisoma trivolvis. Ecography. 2013;36:854–863. doi: 10.1111/j.1600-0587.2013.07868.x. DOI

Zhytova, E. P., Romanchuk, L. D., Guralska, S. V., Andreieva, O. Y. & Shvets, M. V. Circulation pathways of trematodes of freshwater gastropod mollusks in forest biocenoses of the Ukrainian Polissia. Vestn. Zool.53, 13–22 (2019).

Selbach, C. Biology and ecology of trematodes parasitizing aquatic snails in the Ruhr reservoir system in Germany. Doctoral Thesis. (University of Duisburg-Essen, 2016).

Checklist of digeneans (Platyhelminthes, Trematoda, Digenea) of Georgia

Diversity of echinostomes (Digenea: Echinostomatidae) in their snail hosts at high latitudes