Skip to main content
Log in

Elucidation of Himasthla leptosoma (Creplin, 1829) Dietz, 1909 (Digenea, Himasthlidae) life cycle with insights into species composition of the north Atlantic Himasthla associated with periwinkles Littorina spp

  • Genetics, Evolution, and Phylogeny - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Trematodes of the genus Himasthla are usual parasites of coastal birds in nearshore ecosystems of northern European seas and the Atlantic coast of North America. Their first intermediate hosts are marine and brackish-water gastropods, while second intermediate hosts are various invertebrates. We analysed sequences of partial 28S rRNA and nad1 genes and the morphology of intramolluscan stages, particularly cercariae of Himasthla spp. parasitizing intertidal molluscs Littorina spp. in the White Sea, the Barents Sea and coasts of North Norway and Iceland. We showed that only three Himasthla spp. are associated with periwinkles in these regions. Intramolluscan stages of H. elongata were found in Littorina littorea, of H. littorinae, in both L. saxatilis and L. obtusata, and of Cercaria littorinae obtusatae, predominantly, in L. obtusata. Other Himasthla spp. previously reported from Littorina spp. in North Atlantic are either synonymous with one of these species or described erroneously. Based on a comparison of newly generated 28S rDNA sequences with GenBank data, rediae and cercariae of C. littorinae obtusatae were identified as belonging to H. leptosoma. Some previously unknown morphological features of young and mature rediae and cercariae of the three Himasthla spp. are described. We provide a key to the rediae and highlight characters important for identification of cercariae. Genetic diversity within the studied species was only partially determined by their specificity to the molluscan host. The nad1 network constructed for H. leptosoma lacked geographical structure, which is explained by a high gene flow owing to highly vagile definitive hosts, shorebirds.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Bakhmet I, Nikolaev K, Levakin I, Ekimov D (2019) Influence of Himasthla elongata (Trematoda: Echinostomatidae) metacercariae on heart rate in blue mussels (Mytilus edulis). J Invertebr Pathol 166:107220. https://doi.org/10.1016/j.jip.2019.107220

    Article  PubMed  Google Scholar 

  • Bayssade-Dufour C (1979) L’appareil sensorial des cercaires de la systématique des trematodes digénétiques. Mémoir Mus Natl Hist 113:7–75

    Google Scholar 

  • Blakeslee AMH, Byers JE (2008) Using parasites to inform ecological history: comparisons among three congeneric marine snails. Ecology 89(4):1068–1078

    Article  PubMed  Google Scholar 

  • Blasco-Costa I, Poulin R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140:1316–1322

    Article  PubMed  Google Scholar 

  • Blasco-Costa I, Waters JM, Poulin R (2012) Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Mol Ecol 21:207–217

    Article  CAS  PubMed  Google Scholar 

  • Bogéa T (2004) Functional and phylogenetic components in cercarial nervous systems. Folia Parasitol 51:311–319

    Article  Google Scholar 

  • Bogéa T, Caira JN (2001) Ultrastructure and chaetotaxy of sensory receptors in the cercariae of Allassogonoporus sp. Olivier, 1938 (Digenea: Lecithodendriidae). Syst Parasitol 50:1–11

    Article  PubMed  Google Scholar 

  • Bustnes JO, Galaktionov KV (1999) Anthropogenic influences on the infestation of intertidal gastropods by seabird digenean larvae on the southern Barents Sea coast. Mar Biol 133:449–454

    Article  Google Scholar 

  • Bustnes JO, Galaktionov KV, Irwin SWB (2000) Potential threats to littoral biodiversity: is increased parasitism a consequence of human activity? Oikos 90(1):189–190

    Article  Google Scholar 

  • Chapman HD, Wilson RA (1973) The propulation of the cercariae of Himasthla secunda (Nicoll) and Cryptocotyle lingua. Parasitology 67:1–15

    Article  CAS  PubMed  Google Scholar 

  • Chubrik GK (1966) Fauna and ecology of trematode larvae from the molluscs of Barents and White Seas. In: Polyanskiy GI (ed) Life cycles of parasitic worms of northern seas (Proceedings of the Murmansk Marine Biological Institute of the Kola Branch of the USSR Academy of Sciences 10(14)). Nauka, Moscow-Leningrad, pp 78–159 (in Russian)

    Google Scholar 

  • Combescot-Lang C (1976) Etudes des digeneanse s parasites de Littorina saxatilis (Olivi) et de leurs effect sur cet hôte. Ann Parasitol Hum Comp 51:27–36

    Article  CAS  PubMed  Google Scholar 

  • Criscione CD, Blouin MS (2004) Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58(1):198–202

    PubMed  Google Scholar 

  • Criscione CD, Blouin MS (2005) Effective sizes of macroparasite populations: a conceptual model. Trends Parasitol 21(5):212–217

    Article  PubMed  Google Scholar 

  • Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14(8):2247–2257

    Article  CAS  PubMed  Google Scholar 

  • Czubaj A, Niewiadomska K (1988) Types of sensory cells in Notocotylus attenuatus (Rud., 1809) rediae (Digenea, Notocotylidae). Parasitol Res 74:243–249

    Article  Google Scholar 

  • Czubaj A, Niewiadomska K (1996) Ultrastructure of sensory endings in Diplostomum pseudospathaceum Niewiadomska, 1984 cercariae (Digenea: Diplostomidae). Int J Parasitol 26:1217–1225

    Article  CAS  PubMed  Google Scholar 

  • Davies CM, Webster JP, Krüger O, Munatsi A, Ndamba J, Woolhouse MEJ (1999) Host-parasite population genetics: a cross-sectional comparison of Bulinus globosus and Schistosoma haematobium. Parasitology 119:295–302

    Article  PubMed  Google Scholar 

  • Deblock S (1980) Inventaire des trématodes larvaires parasites des mollusques Hydrobia (Prosobranches) des côtes de France. Parassitologia 22:1–105

    CAS  PubMed  Google Scholar 

  • Denisova SA, Shchenkov SV (2020) New data on the nervous system of Cercaria parvicaudata Stunkard & Shaw, 1931 (Trematoda: Renicolidae): revisiting old hypotheses. J Helminthol 94:e52. https://doi.org/10.1017/S0022149X1900035X

    Article  Google Scholar 

  • Desclaux C, de Montaudouin X, Bachelet G (2004) Cockle Cerastoderma edule population mortality: role of the digenean parasite Himasthla quissetensis. Mar Ecol Prog Ser 279:141–150. https://doi.org/10.3354/meps279141

    Article  Google Scholar 

  • Dyachenko V, Beck E, Pantchev N, Bauer C (2008) Cost-effective method of DNA extraction from taeniid eggs. Parasitol Res 102:811–813. https://doi.org/10.1007/s00436-007-0855-6

    Article  CAS  PubMed  Google Scholar 

  • Fried B (2001) Biology of Echinostomes except Echinostoma. Adv Parasitol 49:163–215

    Article  CAS  PubMed  Google Scholar 

  • Galaktionov KV, Bustnes JO (1999) Distribution patterns of marine birds digenean larvae in periwinkles along the southern coast of the Barents Sea. Dis Aquat Org 37:221–230

    Article  CAS  Google Scholar 

  • Galaktionov KV, Dobrovolskij A (2003) The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmissions, and evolution of digenetic trematodes. Kluwer Academic, Boston. https://doi.org/10.1007/978-94-017-3247-5

    Book  Google Scholar 

  • Galaktionov KV, Skírnisson K (2000) Digeneans from intertidal molluscs of SW Iceland. Syst Parasitol 47:87–101

    Article  CAS  PubMed  Google Scholar 

  • Galaktionov KV, Bulat SA, Alekhina IA, Mokrousov IV (2008) Intraspecific genetic variability of microphallids of the “pygmaeus” group (Trematoda, Microphallidae) and possible reasons its determining. In: Galaktionov KV, Dobrovolskij AA (eds) Proceedings of the IV Congress of the Russian Society of Parasitologists – Russian Academy of Sciences, held 20-25 October 2008 at the Zoological Institute RAS, “Parasitology in XXI century – problems, methods, solutions”, vol 1. Lemma, St Petersburg, pp 156–162 (in Russian)

    Google Scholar 

  • Galaktionov KV, Podvyaznaya IM, Nikolaev KE, Levakin IA (2015) Self-sustaining infrapopulation or colony? Redial clonal groups of Himasthla elongata (Trematoda: Echinostomatidae) in Littorina littorea (Gastropoda: Littorinidae) do not support the concept of eusocial colonies in trematodes. Folia Parasitol 62:067. https://doi.org/10.14411/fp.2015.067

    Article  CAS  Google Scholar 

  • Galaktionov NK, Solovyeva AI, Fedorov AV, Podgornaya OI (2014) Trematode Himasthla elongata mariner element (Hemar): structure and applications. J Exp Zool Part B 322:142–155

    Article  CAS  Google Scholar 

  • Galaktionov NK, Podgornaya OI, Strelkov PP, Galaktionov KV (2016) Genomic diversity of cercarial clones of Himasthla elongata (Trematoda: Echinostomatidae) determined with AFLP technique. Parasitol Res 115:4587–4593

    Article  CAS  PubMed  Google Scholar 

  • Ginetsinskaya TA (1968) Trematodes, their life cycles, biology and evolution. Nauka, Leningrad (in Russian) (Translated in 1988 by Amerind Publ Co Pvt Ltd, New Delhi)

    Google Scholar 

  • Gonchar A, Galaktionov KV (2017) Life cycle and biology of Tristriata anatis (Digenea: Notocotylidae): morphological and molecular approaches. Parasitol Res 116(1):45–59. https://doi.org/10.1007/s00436-016-5260-6

    Article  PubMed  Google Scholar 

  • Gonchar A, Galaktionov KV (2020) Short communication: new data support phylogeographic patterns in a marine parasite Tristriata anatis (Digenea: Notocotylidae). J Helminthol 94(e79):1–5. https://doi.org/10.1017/S0022149X19000786

    Article  Google Scholar 

  • Gorbushin AM (2019) Immune response of a caenogastropod host: a case study of Littorina littorea and its digenean parasites. Dev Comp Immunol 101:103465. https://doi.org/10.1016/j.dci.2019.103465

    Article  CAS  PubMed  Google Scholar 

  • Gorbushin AM, Borisova EA (2014) Himasthla elongata: implantation of rediae to the specific iteroparous long-living host, Littorina littorea, results in the immune rejection. Fish Shellfish Immun 39:432–438

    Article  CAS  Google Scholar 

  • Granovitch A, Johannesson K (2000) Digenetic trematodes in four species of Littorina from the west coast of Sweden. Ophelia 53(1):55–65

    Article  Google Scholar 

  • Granovitch AI, Sokolova IM (2001) Littorina arcana Hannaford Ellis, 1978—a new record from the eastern Barents Sea. Sarsia 86:241–243

    Article  Google Scholar 

  • Granovitch AI, Sergievsky SO, Sokolova IM (2000) Spatial and temporal variation of trematode infection in coexisting populations of intertidal gastropods Littorina saxatilis and L. obtusata in the White Sea. Dis Aquat Org 41:53–64

    Article  CAS  Google Scholar 

  • Granovitch AI, Mikhailova NA, Znamenskaya O, Petrova YA (2004) Species complex of mollusks of the genus Littorina (Gastropoda, Prosobranchia) from the Eastern Murman coast. Zool Zh 83(11):1305–1316 (in Russian)

    Google Scholar 

  • Granovitch AI, Maximovich AN, Avanesyan AV, Starunova ZI, Mikhailova NA (2013) Micro-spatial distribution of two sibling periwinkle species across the intertidal indicates hybridization. Genetica 141:293–301 (in Russian)

    Article  PubMed  Google Scholar 

  • Huyse T, Poulin R, Theron A (2005) Speciation in parasites: a population genetics approach. Trends Parasitol 21(10):469–475

    Article  PubMed  Google Scholar 

  • Irwin SWB (1983) Incidence of trematode parasites in two populations of Littorina saxatilis (Olivi) from the north shore of Belfast Lough. Irish Nat J 21:26–29

    Google Scholar 

  • Ishkulov DG, Kuklin VV (1998) On the fauna of Himasthlinae of the Eastern Murman. Parazitologiya 32(1):84–94 (in Russian)

    Google Scholar 

  • James BL (1968) The distribution and keys of species in the family Littorinidae and their digenean parasites, in the region of Dale, Pembrokeshire. Field Stud 2:615–650

    Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28(12):1647–1649. https://doi.org/10.1093/bioinformatics/bts199

    Article  PubMed  PubMed Central  Google Scholar 

  • Kostadinova A (2005) Family Echinostomatidae. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI Publishing and The Natural History Museum, Wallingford and London, pp 9–64

    Chapter  Google Scholar 

  • Kostadinova A, Herniou EA, Barrett J, Littlewood DTJ (2003) Phylogenetic relationships of Echinostoma Rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analyses. Syst Parasitol 54:159–176. https://doi.org/10.1023/A:1022681123340

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lebour MV (1907) Larval trematodes of the Northumberland coast. Trans Nat Hist Soc Northumb (NS) 1:437–454

    Google Scholar 

  • Lebour MV (1908) A contribution to the life-history of Echinostomum secundum Nicoll. Parasitology 1:352–358

    Article  Google Scholar 

  • Lebour MV (1911) A review of the British marine cercariae. Parasitology 4:416–456

    Article  Google Scholar 

  • Lauckner G (1980) Diseases of mollusca: Gastropoda. In: Kinne O (ed) Diseases of marine animals, Protozoa to Gastropoda, vol 1. John Wiley & Sons, New York, pp 311–424

    Google Scholar 

  • Lauckner G (1983) Diseases of mollusca: Bivalvia. In: Kinne O (ed) Diseases of marine animals, vol 2. Biologische Anstalt Helgoland, Hamburg, pp 632–961

    Google Scholar 

  • Lauckner G (1984) Impact of digenean parasitism on the fauna of a North Sea tidal flat. Helgol Wiss Meeresunters 37:185–199

    Article  Google Scholar 

  • Leigh JW, Bryant D (2015) POPART: Full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410

    Article  Google Scholar 

  • Levakin IA, Losev EA, Nikolaev KE, Galaktionov KV (2013a) In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the hemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility. J Helminthol 87:180–188

    Article  CAS  PubMed  Google Scholar 

  • Levakin IA, Nikolaev KE, Galaktionov KV (2013b) Long-term variation in trematode (Trematoda, Digenea) component communities associated with intertidal gastropods is linked to abundance of final hosts. Hydrobiologia 706:103–118

    Article  Google Scholar 

  • Loos-Frank B (1967) Experimentelle Untersuchungen über Bau, Entwicklung und Systematik der Himasthlinae (Trematoda, Echinostomatidae) des Nordseeraumes. Z Parasitenk 28:299–351

    Article  CAS  PubMed  Google Scholar 

  • Magalhães L, Freitas R, de Montaudouin X (2020) How costly are metacercarial infections in a bivalve host? Effects of two trematode species on biochemical performance of cockles. J Invertebr Pathol 177:107479. https://doi.org/10.1016/j.jip.2020.107479

    Article  CAS  PubMed  Google Scholar 

  • Matthews PM, Montgomery WI, Hanna REB (1985) Infestation of littorinids by larval digenea around a small fishing port. Parasitology 90:277–287

    Article  Google Scholar 

  • Morgan JAT, Blair D (1995) Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar-spine group. Parasitology 111:609–615. https://doi.org/10.1017/S003118200007709X

    Article  CAS  PubMed  Google Scholar 

  • Newton I (2003) Speciation and biogeography of birds. Academic Press, Amsterdam, Boston, London et al

    Google Scholar 

  • Newton I (2008) The migration ecology of birds. Academic Press, Amsterdam, Boston, Heidelberg et al

    Google Scholar 

  • Nikolaev KE, Sukhotin AA, Galaktionov KV (2006) Patterns in infection of the White Sea blue mussels (Mytilus edulis L.) of different age and size with metacercariae of digenetic trematodes Himasthla elongata (Mehlis, 1831) (Echinostomatidae) and Cercaria parvicaudata Stunkard & Shaw, 1931 (Renicolidae). Dis Aquat Org 71:51–58

    Article  CAS  Google Scholar 

  • Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755. https://doi.org/10.1016/S0020-7519(03)00049-3

    Article  CAS  PubMed  Google Scholar 

  • Palm HW, Waeschenbach A, Olson PD, Littlewood DTJ (2009) Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Mol Phylogenet Evol 52(2):351–367. https://doi.org/10.1016/j.ympev.2009.01.019

    Article  CAS  PubMed  Google Scholar 

  • Pearson JC (1972) A phylogeny of life-cycle patterns of the Digenea. Adv Parasitol 10:153–189

    Article  CAS  PubMed  Google Scholar 

  • Podvyaznaya IM, Galaktionov KV (2014) Trematode reproduction in the molluscan host: an ultrastructural study of the germinal mass in the rediae of Himasthla elongata (Mehlis, 1831) (Digenea: Echinostomatidae). Parasitol Res 113:1215–1224

    Article  PubMed  Google Scholar 

  • Pohley WJ (1976) Relationships among three species of Littorina and their larval Digenea. Mar Biol 37:179–186

    Article  Google Scholar 

  • Prokofiev VV (2005) Patterns of swimming of cercariae in some trematode species. Parazitologiya 39(3):204–220 (in Russian)

    Google Scholar 

  • Prokofiev VV (2019) Methods effective in the study of chemo-orientation behavior in trematode cercariae. Parazitologiya 53(4):342–347 (in Russian)

    Google Scholar 

  • Prugnolle F, Théron A, Pointier JP, Jabbour-Zahab R, Jarne P, Durand P, Meeûs TD (2005) Dispersal in a parasitic worm and its two hosts: consequence for local adaptation. Evolution 59:296–303

    PubMed  Google Scholar 

  • Rebecq J (1964) Trématodes de Camargue; quelques larves aquatiques et leur écologie. Terre Vie 111:388–392

    Google Scholar 

  • Rees WJ (1936) The effect of parasitism by larval trematodes on the tissues of Littorina littorea (Linne). P Zool Soc Lond 106(2):357–368. https://doi.org/10.1111/j.1469-7998.1936.tb08507.x

    Article  Google Scholar 

  • Reid DG (1996) Systematics and evolution of Littorina. The Ray Society, London

    Google Scholar 

  • Richard J (1971) La chétotaxie des cercaries. Valeur systématique et phylétique. Mémoir Mus Natl Hist 67:4–177

    Google Scholar 

  • Ronquist F, Huelsenbeck J, Teslenko M (2011) MrBayes Version 3.2 Manual: Tutorials and Model Summaries

    Google Scholar 

  • Skírnisson K, Galaktionov KV (2002) Life cycles and transmission patterns of seabird digeneans in SW Iceland. Sarsia 87:144–151

    Article  Google Scholar 

  • Solovyeva AI, Stefanova VN, Podgornaya OI, Siu D (2016) Karyotype features of trematode Himasthla elongata. Mol Cytogenet 9:34. https://doi.org/10.1186/s13039-016-0246-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Solovyeva A, Nikolaev K, Lebedev E, Potolytsina E, Galaktionov N, Levakin I (2020) Reduced infectivity in Himasthla elongata (Trematoda, Himasthlidae) cercariae with deviant photoreaction. J Helminthol 94(e129):1–5. https://doi.org/10.1017/S0022149X20000103

    Article  Google Scholar 

  • Stunkard HW (1938) The morphology and life-cycle of the trematode, Himasthla quissetensis (Miller and Northup, 1926). Biol Bull 75:145–164

    Article  Google Scholar 

  • Stunkard HC (1960) Further studies on the trematode genus Himasthla with descriptions of H. mcintoshi n. sp., H. piscicola n. sp., and stages in the life history of H. compacta n. sp. Biol Bull 119:529–549

    Article  Google Scholar 

  • Stunkard HW (1966) The morphology and life history of the digenetic trematode, Himasthla littorinae sp. n. (Echinostomatidae). J Parasitol 52:367–372

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thieltges DW (2006) Effect of infection by the metacercarial trematode Renicola roscovita on growth in intertidal blue mussel Mytilus edulis. Mar Ecol Prog Ser 319:129–134

    Article  Google Scholar 

  • Thieltges DW, Fredensborg BL, Poulin R (2009a) Geographical variation in metacercarial levels in marine invertebrate hosts: parasite species character versus local factors. Mar Biol 156:983–990

    Article  Google Scholar 

  • Thieltges DW, Reise K, Prinz K, Jensen KT (2009b) Invaders interfere with native parasite–host interactions. Biol Invasions 11:1421–1429

    Article  Google Scholar 

  • Timon-David J, Rebecq J (1958) Les métacercaires parasites de l'annélide Nereis diversicolor O. F. Miiller et leur développement expérimental. Compt Rend Séanc Soc Biol 152:1731–1733

    CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Toledo R, Esteban JG, Fried B (2012) Current status of food-borne trematode infections. Eur J Clin Microbiol Infect Dis 31:1705–1718. https://doi.org/10.1007/s10096-011-1515-4

    Article  CAS  PubMed  Google Scholar 

  • Vanoverschelde R, Vaes P (1980) Studies on the life-cycle of Himasthla militaris (Trematoda: Echinostomatidae). Parasitology 81:609–617

    Article  Google Scholar 

  • Vázquez-Prieto S, Vilas R, Paniagua E, Ubeira FM (2015) Influence of life history traits on the population genetic structure of parasitic helminths: a minireview. Folia Parasitol 62:060

    Article  Google Scholar 

  • Wegeberg AM, Jensen KT (1999) Reduced survivorship of Himasthla (Trematoda, Digenea)-infected cockles (Cerastoderma edule) exposed to oxygen depletion. J Sea Res 42:325–331. https://doi.org/10.1016/S1385-1101(99)00035-0

    Article  Google Scholar 

  • Wegeberg AM, Jensen KT (2003) In situ growth of juvenile cockles, Cerastoderma edule, experimentally infected with larval trematodes (Himasthla interrupta). J Sea Res 50:37–43. https://doi.org/10.1016/S1385-1101(03)00042-X

    Article  Google Scholar 

  • Werding B (1969) Morphologie, Entwicklung und Ökologie digener Trematoden-Larven der Strandschnecke Littorina littorea. Mar Biol 3:306–333

    Article  Google Scholar 

  • Williams IC, Ellis C (1976) Larval Digenea in Shetland. Glasg Nat 19:307–315

    Google Scholar 

  • Winnepenninckx B, Backeljau T, De Wachter R (1993) Extraction of high molecular weight DNA from molluscs. Trends Genet 9(12):407. https://doi.org/10.1016/0168-9525(93)90102-n

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the White Sea Biological Station of the Zoological Institute of the Russian Academy of Sciences (ZIN RAS) for providing fieldwork infrastructure. We thank Anna Gonchar, Dr. Kirill Nikolaev and Dr. Ivan Levakin for their help with sampling and primary treatment of the material. Sampling in Iceland would have been impossible without the support of Dr. Karl Skírnisson. We would also like to thank the “Taxon” Research Resource Center (http://www.ckp-rf.ru/ckp/3038/) of ZIN RAS and the research resource centre “Molecular and Cell Technologies” of Saint-Petersburg State University for granting access to their facilities. We are grateful to Natalia Lentsman for her help with the manuscript preparation.

Funding

The fieldwork at the White Sea Biological Station and at the “Taxon” Research Resource Center was partly financed by the research programme of Zoological Institute RAS, project number AAAA-A19-119020690109-2. The treatment and analysis of the accumulated data were supported by the Russian Science Foundation (Grant No. 18-14-00170).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kirill V. Galaktionov.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Christoph G. Grevelding

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Galaktionov, K.V., Solovyeva, A.I. & Miroliubov, A. Elucidation of Himasthla leptosoma (Creplin, 1829) Dietz, 1909 (Digenea, Himasthlidae) life cycle with insights into species composition of the north Atlantic Himasthla associated with periwinkles Littorina spp. Parasitol Res 120, 1649–1668 (2021). https://doi.org/10.1007/s00436-021-07117-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-021-07117-8

Keywords

Navigation