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Prey-mimetism in cercariae of Apatemon (Digenea, Strigeidae) in freshwater in northern latitudes

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Abstract

Cercariae, the free-living larval stages of trematodes, have adopted an amazing variety of transmission strategies. One of them is prey-mimetism, i.e. cercariae mimicking prey to attract motile hosts to be eaten. In a period between 2002 and 2019, we examined small planorbid snails, Bathyomphalus contortus, Gyraulus parvus and Planorbis planorbis from lakes in Finland and Iceland and from the Curonian Lagoon in Lithuania. Cercariae with conspicuously enlarged tails and unusual swimming behaviour, likely mimicking invertebrate prey, were detected and studied by the use of morphological and molecular (cox1, ITS1-5.8S-ITS2 and 28S rDNA) methods. Cercariae of two species belonging to the genus Apatemon (Strigeidae) were recognised. We consider Apatemon sp. 5 ex P. planorbis from the Curonian Lagoon identical to Cercaria globocaudata U. Szidat, 1940. Cercariae ex G. parvus from Iceland and ex B. contortus from Finland were conspecific, and we named them Apatemon sp. 6; these cercariae could not be associated with any known species. For the first time, we verified that cercariae of the Bulbocauda group belong to the genus Apatemon. We provide a mini-review on records of furcocercariae of the family Strigeidae with enlarged tails reported in freshwaters of the northern hemisphere and reveal that it is not only Apatemon but also Australapatemon and most likely Strigea which belong to the Bulbocauda group, rendering it a purely ecological assemblage. Understanding which invertebrate swimming behaviour these cercariae are mimicking will enhance our knowledge of the processes behind trematode transmission and will help to assess evolutionary pathways of host-finding strategies in trematodes.

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Data availability

Data are available from the authors upon reasonable request; sequences are available via GenBank.

References

  • Adalsteinsson H (1979) Size and food of arctic char Salvelinus alpinus and stickleback Gasterosteus aculeatus in Lake Mývatn. Oikos 32:228–231. https://doi.org/10.2307/3544229

    Article  Google Scholar 

  • Beckerdite FW, Miller GC, Harkema R (1971) Observations on the life cycle of Pharyngostomides spp. and the description of P. adenocephala sp. n. (Strigeiodea: Diplostomidae) from the raccoon, Procyon lotor (L.). Proc Helm Soc Wash 38:149–156

    Google Scholar 

  • Belyakova YV, Mazina VV (1987) A new furcocercaria, Cercaria kazakhstanica IX sp. n., from water bodies of Kazakhstan. Parazitologiya 21:501–504

    Google Scholar 

  • Bhatnagar S, Saxena SK (1982) On a furcocercaria Cercaria kukrailensis I sp. n. with a bulbous tail. Helminthologia 19:219–225

    Google Scholar 

  • Blair D (1976) Observations of the life-cycle of the strigeoid trematode, Apatemon (Apatemon) gracilis (Rudolphi, 1819) Szidat, 1928. J Helminthol 50:125–131. https://doi.org/10.1017/s0022149x00027607

    Article  CAS  PubMed  Google Scholar 

  • Blair D (1977) A key to cercariae of British strigeoids (Digenea) for which the life-cycles are known, and notes on the characters used. J Helminthol 51:155–166. https://doi.org/10.1017/s0022149x00007434

    Article  CAS  PubMed  Google Scholar 

  • Blasco-Costa I, Cutmore SC, Miller TL, Nolan MJ (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Syst Parasitol 93:295–306. https://doi.org/10.1007/s11230-016-9631-2

    Article  PubMed  Google Scholar 

  • Blasco-Costa I, Poulin R, Presswell B (2016) Species of Apatemon Szidat, 1928 and Australapatemon Sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: linking and characterising life cycle stages with morphology and molecules. Par Res 115:271–289. https://doi.org/10.1007/s00436-015-4744-0

    Article  Google Scholar 

  • Born-Torrijos A, Paterson RA, van Beest GS, Vyhlídalová T, Henriksen EH, Knudsen R, Kristoffersen R, Amundsen PA, Soldánová M (2021) Cercarial behaviour alters the consumers functional response of three-spined sticklebacks. J Anim Ecol 90:978–988. https://doi.org/10.1111/1365-2656.13427

    Article  PubMed  Google Scholar 

  • Butorina TE (1988) A new furcocercaria from freshwater lakes of Kamtchatka. Parazitologiya 22:247–249. (in Russian)

    Google Scholar 

  • Butorina TE, Sinebokova MBK (1986) On the fauna of larval trematodes from freshwater molluscs of Kamtchatka. Helminths and the diseases caused by them, DVNTSAN SSSR, Vladivostok, 67–78. (in Russian)

  • Christensen NO, Frandsen F, Nansen P (1980) The interaction of some environmental factors influencing Schistosoma mansoni cercarial host-finding. J Helminthol 54:203–5. https://doi.org/10.1017/S0022149X0000660X

    Article  CAS  PubMed  Google Scholar 

  • Combes C, Fournier A, Moné H, Théron A (1994) Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109S:S3–S13. https://doi.org/10.1017/s0031182000085048

    Article  Google Scholar 

  • Combes C, Bartoli P, Théron A (2002) Trematode transmission strategies. In: Lewis EE, Campbell JF, Sukhdeo MVK (eds) The Behavioural Ecology of Parasites. CAB International, Wallingford, pp 1–12

    Google Scholar 

  • Combes C (1980) Les mécanismes de recrutement chez les metazoaires parasites et leur interpretation en termes de strategies démographiques. Vie et Milieu 30:55–63. https://hal.sorbonne-universite.fr/hal-03007880

  • Cribb TH (2002) Superfamily Bivesiculoidea Yamaguti, 1934. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda. Vol 1. CAB International and The Natural History Museum, Wallingford, London, pp 25–29

  • Cribb TH, Bray RA, Olson PD, Littlewood DTJ (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254. https://doi.org/10.1016/s0065-308x(03)54004-0

    Article  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois G (1968) Synopsis des Strigeidae et des Diplostomatidae (Trematoda). Mém Soc Neuchateloise Sci Nat 10:1–259

    Google Scholar 

  • Fain A (1953) Contribution à l‘étude des formes larvaires des Trématodes au Congo Belge et spécialement de la larve de Schistosoma mansoni. Mémoirs Institute Royal Colonial Belge. Section des Sciences Naturelles et Médicales 8:1–312

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Faltýnková A, Valtonen ET, Karvonen A (2008) Spatial and temporal structure of the trematode component community in Valvata macrostoma (Gastropoda, Prosobranchia). Parasitology 135:1691–1699. https://doi.org/10.1017/S0031182008005027

    Article  PubMed  Google Scholar 

  • Faltýnková A, Kudlai O, Pantoja C, Yakovleva G, Lebedeva D (2022) Another plea for ‘best practice’ in molecular approaches to trematode systematics: Diplostomum sp. clade Q identified as Diplostomum baeri Dubois, 1937 in Europe. Parasitology 149:503–518. https://doi.org/10.1017/S0031182021002092

    Article  CAS  PubMed  Google Scholar 

  • Fernández MV, Hamann MI, Ostrowski-de Núñez M (2013) Larval trematodes of Biomphalaria straminea (Mollusca: Planorbidae) in a ricefield in Corrientes Province, Argentina. Rev Mex Biodivers 84:756–764. https://doi.org/10.7550/rmb.33748

    Article  Google Scholar 

  • Fernández MV, Hamannn MI, Ostrowski de Núñez M (2016) New larval trematodes in Biomphalaria species (Planorbidae) from Northeastern Argentina. Acta Parasitol 61:471–492. https://doi.org/10.1515/ap-2016-0064

    Article  PubMed  Google Scholar 

  • Fernández J, Esch GW (1991) The component community structure of larval trematodes in the pulmonate snail Helisoma anceps. J Parasitol 77:540–550. https://www.jstor.org/stable/3283157

  • Froese R, Pauly D (2022) FishBase. World Wide Web electronic publication. Available at www.fishbase.org. Accessed 08/2022.

  • Galaktionov KV, Dobrovolskiy AA (2003) The biology and evolution of trematodes. An essay on the biology, morphology, life cycles, transmission and evolution of digenetic trematodes. Kluwer Academic Publishers, Boston, Dordrecht, London

  • Galazzo DE, Dayanandan S, Marcogliese DJ, McLaughlin JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNAsequence data and comparisons with European congeners. Can J Zool 80:2207–2217. https://doi.org/10.1139/z02-198

    Article  CAS  Google Scholar 

  • Garey JR, Wolstenholme DR (1989) Platyhelminth mitochondrial DNA: evidence for early evolutionary origin of a tRNA ser AGN that contains a dihydrouridine arm replacement loop, and of serine-specifying AGA and AGG codons. J Mol Evol 28:374–387. https://doi.org/10.1007/BF02603072

    Article  CAS  PubMed  Google Scholar 

  • Georgieva S, Kostadinova A, Skírnisson K (2012) The life-cycle of Petasiger islandicus Kostadinova & Skírnisson, 2007 (Digenea: Echinostomatidae) elucidated with the aid of molecular data. Syst Parasitol 82:177–183. https://doi.org/10.1007/s11230-012-9354-y

    Article  PubMed  Google Scholar 

  • Ginetsinskaya TA (1968) Trematodes, their life cycles, biology and evolution. Izdatelstvo Nauka, Leningradskoe Otdelenie, Leningrad. (in Russian)

  • Gíslason GM, Gudmundsson Á, Einarsson Á (1998) Population densities of three-spined sticklebacks (Gasterosteus aculeatus L.) in a shallow lake. Int Ver theor angew Limnol: Verh 26:2244–2250. https://doi.org/10.1080/03680770.1995.11901146

    Article  Google Scholar 

  • Glöer P (2002) Die Süßwassergastropoden Nord-und Mitteleuropas. Bestimmungschlüssel, Lebensweise, Verbreitung. Die Tierwelt Deutschlands, Teil 73. ConchBooks, Hackenheim

  • Goedknegt A, Welsh J, Thieltges DW (2012) Parasites as prey. In: eLS. (Eds: J. Wiley & Sons). Ltd: Chichester. https://doi.org/10.1002/9780470015902.a0023604

  • Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  • Hoberg EP, Galbreath KE, Cook JA, Kutz SJ, Polley L (2012) Northern host parasite assemblages: history and biogeography on the borderlands of episodic climate and environmental transition. Adv Parasitol 79:1–97. https://doi.org/10.1016/B978-0-12-398457-9.00001-9

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Huston DC, Ogawa K, Shirakashi S, Nowak BF (2020) Metazoan parasite life cycles: significance for fish mariculture. Trends Parasitol 36:1002–1012. https://doi.org/10.1016/j.pt.2020.07.011

    Article  PubMed  Google Scholar 

  • Hynes HBN (1950) The food of fresh-water sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius), with a review of methods used in studies of the food of fishes. J Anim Ecol 19:36–58

    Article  Google Scholar 

  • Ibrahim AA, Huntingford FA (1989) Laboratory and field studies on diet choice in three-spined sticklebacks, Gasterosteus aculeatus L., in relation to profitability and visual features of prey. J Fish Biol 34:245–257. https://doi.org/10.1111/j.1095-8649.1989.tb03306.x

    Article  Google Scholar 

  • Jóhannesdóttir L, Arnalds Ó, Brink S, Gunnarsson TG (2014) Identifying important bird habitats in a sub-Arctic area undergoing rapid land-use change. Bird Study 61:544–552. https://doi.org/10.1080/00063657.2014.962481

    Article  Google Scholar 

  • Johnson PTJ, Dobson A, Lafferty KD, Marcogliese JD, Memmott J, Orlofske SA, Poulin R, Thieltges DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol 25:362–371. https://doi.org/10.1016/j.tree.2010.01.005

    Article  PubMed  Google Scholar 

  • Kaplan AT, Rebhal S, Lafferty KD, Kuris AM (2009) Small estuarine fishes feed on large trematode cercariae: lab and field investigations. J Parasitol 95:477–480. https://doi.org/10.1645/GE-1737.1

    Article  PubMed  Google Scholar 

  • Karvonen A, Faltýnková A, Mah Choo J, Valtonen ET (2017) Infection, specificity and host manipulation of Australapatemon sp. (Trematoda, Strigeidae) in two sympatric species of leeches (Hirudinea). Parasitology 144:1346–1355. https://doi.org/10.1017/S0031182017000609

    Article  PubMed  Google Scholar 

  • Kudlai O, Pantoja C, O’Dwyer K, Jouet D, Skírnisson K, Faltýnková A (2021) Diversity of Plagiorchis (Trematoda: Digenea) in high latitudes: species composition and snail host spectrum revealed by integrative taxonomy. J Zool Syst Evol Res 59:937–962. https://doi.org/10.1111/jzs.12469

  • Kuris AM, Hechinger R, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, Dobson AP, Dunham EJ, Fredensborg BL, Huspeni TC, Lorda J, Mababa L, Mancini FT, Mora AB, Pickering M, Talhouk ND, Torchin ME, Lafferty KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454:515–518. https://doi.org/10.1038/nature06970

    Article  CAS  PubMed  Google Scholar 

  • Lafferty KD, Dobson AP, Kuris AM (2006) Parasites dominate food web links. Proc Natl Acad Sci USA 103:1211–6. https://doi.org/10.1073/pnas.0604755103

    Article  CAS  Google Scholar 

  • Leung TLF, Koprivnikar J (2016) Nematode parasite diversity in birds: the role of host ecology, life history and migration. J Anim Ecol 85:1471–1480. https://doi.org/10.1111/1365-2656.12581

    Article  PubMed  Google Scholar 

  • Lewis MC, Welsford IG, Uglem GL (1989) Cercarial emergence of Proterometra macrostoma and P. edneyi (Digenea: Azygiidae): contrasting responses to light: dark cycling. Parasitology 99:215–223. https://doi.org/10.1017/S0031182000058662

    Article  Google Scholar 

  • Locke SA, McLaughlin D, Marcogliese DJ (2010) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River. Canada. Mol Ecol 19:2813–2827. https://doi.org/10.1111/j.1365-294X.2010.04713.x

    Article  CAS  PubMed  Google Scholar 

  • Locke SA, Drago FB, López-Hernández D, Chibwana FD, Núñez V, Van Dam A, Achinelly MF, Johnson PTJ, Alves Costa, de Assis J, Lane de Melo A, Pinto HA (2021) Intercontinental distributions, phylogenetic position and life cycles of species of Apharyngostrigea (Digenea, Diplostomoidea) illuminated with morphological, experimental, molecular and genomic data. Int J Parasitol 51:667–683. https://doi.org/10.1016/j.ijpara.2020.12.006

    Article  CAS  PubMed  Google Scholar 

  • López-Hernández D, Locke SA, Alves de Cassis JC, Drago FB, Lane de Melo A, Rabelo ÉML, Pinto HA (2019) Molecular, morphological and experimental-infection studies of cercariae of five species of the superfamily Diplostomoidea (Trematoda: Digenea) infecting Biomphalaria straminea (Mollusca: Planorbidae) in Brazil. Acta Trop 199:105082. https://doi.org/10.1016/j.actatropica.2019.105082

    Article  CAS  PubMed  Google Scholar 

  • Lorencová E, Beran L, Nováková M, Horsáková V, Rowson B, Hlaváč JČ, Nekola JC, Horsák M (2021) Invasion at the population level: a story of the freshwater snails Gyraulus parvus and G. laevis. Hydrobiologia 848:4661–4671. https://doi.org/10.1007/s10750-021-04668-w

    Article  Google Scholar 

  • Louhi KR, Karvonen A, Rellstab C, Jokela J (2010) Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile host? Infect Genet Evol 10:1271–1277. https://doi.org/10.1016/j.meegid.2010.08.013

    Article  PubMed  Google Scholar 

  • Lutz A (1931) Contribution to the knowledge of the ontogeny of Strigeids. Mem Inst Oswaldo Cruz 25:333–353. (in Portuguese)

    Article  Google Scholar 

  • Miller HM (1925) The larval trematode infestation of the freshwater mollusks of San Juan Island, Puget Sound. Washington University Studies, Scientific Series 13:9–22

    Google Scholar 

  • Miller HM (1927) Furcocercous larval trematodes from San Juan Island Washington. Parasitology 19:61–83. https://doi.org/10.1017/S0031182000005539

    Article  Google Scholar 

  • Mironova E, Gopko M, Pasternak A, Mikheev V, Taskinen J (2019) Trematode cercariae as prey for zooplankton: effect on fitness traits of predators. Parasitology 146:105–111. https://doi.org/10.1017/S0031182018000963

    Article  PubMed  Google Scholar 

  • Morley NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691:7–19. https://doi.org/10.1007/s10750-012-1029-9

    Article  CAS  Google Scholar 

  • Morton DN, Lafferty KD (2022) Parasites in kelp-forest food webs increase food-chain length, complexity, and specialization, but reduce connectance. Ecol Monogr 92:1506. https://doi.org/10.1002/ecm.1506

    Article  Google Scholar 

  • Moszczynska A, Locke SA, McLaughlin JD, Marcogliese DJ, Crease TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Mol Ecol Resour 9:S75–S82. https://doi.org/10.1111/j.1755-0998.2009.02634.x

    Article  CAS  Google Scholar 

  • Mukherjee RP (2007) Fauna of India and the adjacent countries. Larval Trematode. Distome furcocercous cercariae. Part III. Zoological Survey of India. M-Block, New Alipore, Kolkata

  • Nasir P, Diaz MT (1973) Freshwater larval trematodes. XXXII. Twenty new species of Venezuelan cercariae. Riv Parassitol 34:1–44

    Google Scholar 

  • Nasiг P (1973) Freshwater larval trematodes XXXII. Twenty new species of Venezuelan cercariae. Riv Parassitol 34:24–25

    Google Scholar 

  • Nassi H (1987) Sur quatre furcocercaires émises par Biomphalaria glabrata en Guadeloupe. Annales de Parasitologie Humaine et Comparée 62:17–35. https://doi.org/10.1051/PARASITE/198762117

    Article  Google Scholar 

  • Niewiadomska K (1966) A new species of furcocercaria, Cercaria notabilis sp. n., from the Mazurian Lakes. Acta Parasitol Polonica 14:21–25

    Google Scholar 

  • Niewiadomska K (1970) Cercaria clavicauda sp. n. – a new species of furcocercaria from the Mazurian lakes. Acta Parasitol Polon 18:341–346

    Google Scholar 

  • Niewiadomska K (1981) New species of furcocercaria, Cercaria cyclopoides sp. n. from Mazurian Lakes. Poland. Acta Parasitol Polon 28:117–123

    Google Scholar 

  • Niewiadomska K, Kiseliene V (1993) General morphology and SEM ultrastructure of Cercaria globocaudata U. Szidat, 1940 (Digenea). Acta Parasitol 38:62–68

    Google Scholar 

  • Ohama T, Osawa S, Watanabe K, Jukes TH (1990) Evolution of the mitochondrial genetic code IV. AAA as an asparagine codon in some animal mitochondria. J Mol Evol 30:329–332. https://doi.org/10.1007/BF02101887

    Article  CAS  PubMed  Google Scholar 

  • Olivier L (1940) Life history studies on two strigeid trematodes of the Douglas Lake Region, Michigan. J Parasitol 26:447–477. https://doi.org/10.2307/3272250

    Article  Google Scholar 

  • Orlofske SA, Jadin RC, Johnson PTJ (2015) It’s a predator–eat–parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178:537–547. https://doi.org/10.1007/s00442-015-3243-4

    Article  PubMed  Google Scholar 

  • Orlovskaya OM (1984) Cercaria tschaunensis sp. n. (Trematoda) from waters of North-Western Chukotka. Parazitologiya 18:325–328. (in Russian)

  • Ostrowski de Núñez M (1989) The life history of a trematode, Apharyngostrigea simplex (Johnston 1904), from the ardeid bird Egretta thula in Argentina. Zool Anz 5:322–336

    Google Scholar 

  • Paepke HJ (2001) Gasterosteus aculeatus Linnaeus, 1758. In: Banarescu P, Paepke HJ (eds) The freshwater fishes of Europe Cyprinidae, vol. 5. Aula-Verlag, Wiebelsheim

  • Pantoja C, Faltýnková A, O’Dwyer K, Jouet D, Skírnisson K, Kudlai O (2021) Diversity of echinostomes (Digenea: Echinostomatidae) in their snail hosts at high latitudes. Parasite 28:59. https://doi.org/10.1051/parasite/2021054

  • Paulauskas A, Rosef O, Galdikaite E, Radzijevskaja J (2009) Infestation with Ixodes ricinus ticks on migrating passerine birds in Lithuania and Norway. Acta Biol Univ Daugavpiliensis 9:1–6

    Google Scholar 

  • Pleijel F, Jondelius U, Norlinder E, Nygren A, Oxelman B, Schander C, Sundberg P, Thollesson M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phylogenet Evol 48:369–371. https://doi.org/10.1016/j.ympev.2008.03.024

    Article  CAS  PubMed  Google Scholar 

  • Presswell B (2022) New specimens and molecular data provide validation of Apatemon jamiesoni n. sp. (Trematoda: Strigeidae) from water birds in New Zealand. Syst Parasitol 99:553–543. https://doi.org/10.1007/s11230-022-10043-7

    Article  Google Scholar 

  • Prokofiev VV, Galaktionov KV (2009) Strategies of search behaviour in trematode cercariae. Tr Zool Inst RAN 313:308–318. https://doi.org/10.31610/trudyzin/2009.313.3.308 (In Russian)

  • Rambaut A, Suchard M, Xie W, Drummond A (2014) Tracer v. 1.6. University of Edinburgh, Institute of Evolutionary Biology, Edinburgh https://beast.bio.ed.ac.uk/Tracer. Accessed 26 Nov 2016

  • Rambaut A (2012) Institute of evolutionary biology. Molecular evolution, phylogenetics and epidemiology. University of Edinburgh Vol. FigTree v1 (p. 4)

  • Robinson JA (1999) Migration and morphometrics of the red-breasted merganser Mergus serrator in northern Eurasia and the implications for conservation of this species in Britain and Ireland. Wildfowl 50:139–148

    Google Scholar 

  • Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwelm J, Soldánová M, Vyhlídalová T, Sures B, Selbach C (2018) 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 117:241–255. https://doi.org/10.1007/s00436-017-5699-0

    Article  CAS  PubMed  Google Scholar 

  • Seppälä O, Karvonen A, Valtonen ET (2006) Susceptibility of eye fluke-infected fish to predation by bird hosts. Parasitology 132:575–579. https://doi.org/10.1017/S0031182005009431

    Article  PubMed  Google Scholar 

  • Singh RN (1952) Studies on strigeid cercariae from northern India II A new species of strigeid cercaria, Cercaria sphericauda from Indoplanorbis exustus. Proc Natl Acad Sci India, Sect B, Biol Sci 22:12–21

    Google Scholar 

  • Skírnisson K, Galaktionov KV, Kozminsky V (2004) Factors influencing the distribution of digenetic trematode infections in a mudsnail (Hydrobia ventrosa) population inhabiting salt marsh ponds in Iceland. J Parasitol 90:50–59. https://doi.org/10.1645/GE-118R

    Article  PubMed  Google Scholar 

  • Smith N (2001) Spatial heterogeneity in recruitment of larval trematodes to snail intermediate hosts. Oecologia 127:115–122. https://doi.org/10.1007/s004420000560

    Article  PubMed  Google Scholar 

  • Soldánová M, Georgieva S, Roháčová J, Knudsen R, Kuhn JA, Henriksen EH, Amundsen PA (2017) Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. Int J Parasitol 47:327–345. https://doi.org/10.1016/j.ijpara.2016.12.008

    Article  CAS  PubMed  Google Scholar 

  • Szidat U (1940) Neue Cercarienstudien. Zentralbl Bakteriol Parasitenkd Infekt Krankh 145:438–448

    Google Scholar 

  • Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thieltges DW, de Montaudouin X, Fredensborg B, Jensen KT, Koprivnikar J, Poulin R (2008) Production of marine trematode cercariae – a potentially overlooked path of energy flow in benthic systems. Mar Ecol Progr Ser 372:147–155. https://doi.org/10.3354/meps07703

    Article  Google Scholar 

  • Thieltges DW, Amundsen PA, Hechinger RF, Johnson PTJ, Lafferty KD, Mouritsen KN, Preston DL, Reise K, Zander CD, Poulin R (2013) Parasites as prey in aquatic food webs: implications for predator infection and parasite transmission. Oikos 122:1473–1482. https://www.jstor.org/stable/24567379

  • Timm T, Martin PJ (2015) Chapter 21 – Clitellata: Oligochaeta. In: Thorp JH, Rogers DC (eds) Thorp and Covich’s freshwater invertebrates, ecology and general biology. 4th edn. Academic Press, Amsterdam

  • Vojtek J (1964) The importance of life-history studies for the systematics of the genus Apatemon (Trematoda, Strigedae). In: Ergens R, Ryšavý B (eds) Parasitic worms and aquatic conditions. Proceedings of symposium, Prague, October 29 – November 2, 1962, Publishing House of Czech Academy of Sciences, Prague, pp 121–130

  • Yamaguti S (1975) Synoptical review of life histories of digenetic trematodes of vertebrates with special reference to the morphology of their larval forms. Keigaku Publishing Co, Tokyo

    Google Scholar 

  • Žiliukas V (2003) Assessment of the dynamics of main ecological parameters of the fish fry community in the coastal zone of the Curonian Lagoon near Vente Cape. Acta Zool Litu 13:167–175. https://doi.org/10.1080/13921657.2003.10512560

    Article  Google Scholar 

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Acknowledgements

The present study was funded by the research fund from the University of Iceland and the Czech Grant Agency (project No. 18-18597S). We are grateful to Blanka Škoríková for the scanning and processing of drawings.

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Authors and Affiliations

  1. Department of Forest Ecology, Faculty of Forestry and Wood Technology, Mendel University in Brno, Zemědělská 3, Brno, 613 00, Czech Republic

    Anna Faltýnková

  2. Institute of Parasitology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic

    Anna Faltýnková

  3. Institute of Ecology, Nature Research Centre, Akademijos 2, 08412, Vilnius, Lithuania

    Olena Kudlai & Camila Pantoja

  4. BioSpecT EA7506, Faculty of Pharmacy, University of Reims Champagne-Ardenne, 51 rue Cognacq-Jay, 51096, Reims Cedex, France

    Damien Jouet

  5. Laboratory of Parasitology, Institute for Experimental Pathology, Keldur, University of Iceland, IS-112, Reykjavík, Iceland

    Karl Skírnisson

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  1. Anna Faltýnková
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Contributions

Conceptualisation: AF, OK and KS. Developing methods and data analysis: AF, OK, CP and DJ. The preparation of figures and tables: AF and OK. Conducting the research, data interpretation and writing: AF, OK, CP, DJ and KS.

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Correspondence to Olena Kudlai.

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Faltýnková, A., Kudlai, O., Pantoja, C. et al. Prey-mimetism in cercariae of Apatemon (Digenea, Strigeidae) in freshwater in northern latitudes. Parasitol Res 122, 815–831 (2023). https://doi.org/10.1007/s00436-023-07779-6

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