Advertisement

Parasitology Research

, Volume 116, Issue 1, pp 45–59 | Cite as

Life cycle and biology of Tristriata anatis (Digenea: Notocotylidae): morphological and molecular approaches

Original Paper

Abstract

Notocotylids are common digeneans parasitising birds and mammals. They have a two-host life cycle with cercariae encysting in the open. Particular life cycles remain unknown for majority of notocotylid species, including a common parasite of sea ducks Tristriata anatis. Here we resolve the life cycle of T. anatis by means of D2 LSU, ITS1 and CO1 DNA sequence analysis, showing that the first intermediate hosts for this species are periwinkles Littorina spp. Morphological descriptions of rediae and cercariae are provided for the first time, and we also supplement the existing morphological data on adults. Apart from differential diagnosis, we discuss some features of cercariae and rediae biology, geographical distribution and host range. Our molecular data confirm that genus Tristriata is monotypic and that T. anatis has circumpolar distribution. CO1 sequence analysis has shown that isolation exists between the Atlantic and Pacific populations of T. anatis, suggesting that there are geographical races. We suppose that their formation may be linked to the Last Ice Age events, when trans-Arctic bird migrations ceased and periwinkle ranges shrunk. These made transfer of parasites across the Arctic impossible, and it still has not resumed. We discuss the possible influence of host vagility and adults’ lifespan on digeneans’ potential for geographical colonisation.

Keywords

Digenea Notocotylidae Trematode Marine parasites Life cycle Phylogeography Circumpolar distribution Parthenitae 

Notes

Acknowledgments

This study was funded by the Russian Science Foundation (grant number 14-14-00621). We are grateful to Karl Skírnisson, Andrei Granovitch, Daria Aleshkina and Ksenia Volovik for providing samples from certain locations, and Damien Jouet, above that, for his great assistance in parts of the work. Field research was largely based at the White Sea Biological Station of the Zoological Institute of the Russian Academy of Sciences (ZIN RAS), and molecular research at the Laboratory of molecular systematics ZIN RAS. Part of the sequencing was performed at the research resource centre “Molecular and cell technologies” (St Petersburg State University).

References

  1. Alerstam T, Bäckman J, Gudmundsson GA, Hedenström A, Henningsson SS, Karlsson H, Strandberg R (2007) A polar system of intercontinental bird migration. Proc R Soc Lond B Biol Sci 274(1625):2523–2530CrossRefGoogle Scholar
  2. Andreev AV, Kondratiev AV (2001) Birds of the Koni-Pyagyn and Malkachan areas. In: Biodiversity and ecological status of the northern coast of the Sea of Okhotsk. Vladivostok, p 87–122 (in Russian)Google Scholar
  3. Bartoli P, Jousson O, Russell-Pinto F (2000) The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data. J Parasitol 86:479–489CrossRefPubMedGoogle Scholar
  4. Belopolskaia MM (1952) Parasite fauna of marine waterfowl. Scientific reports of LSU 141(28):127–180 (in Russian)Google Scholar
  5. Belopolskaia MM (1953) In: Skrjabin KI (ed) Trematodes of Animals and Man: Fundamentals of Trematodology, vol. 8. USSR Academy of Sciences Publishing, Moscow, p 132, 137, 139 (in Russian)Google Scholar
  6. Bowles J, Hope M, Tiu WU, Liu X, McManus DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Trop 55:217–229CrossRefPubMedGoogle Scholar
  7. Bowles J, McManus DP (1993) Molecular variation in Echinococcus. Acta Trop 53(3):291–305CrossRefPubMedGoogle Scholar
  8. Buehler DM, Baker AJ, Piersma T (2006) Reconstructing palaeoflyways of the late Pleistocene and early Holocene Red Knot Calidris canutus. Ardea-Wageningen 94(3):485Google Scholar
  9. Bustnes JO, Mosbech A, Sonne C, Systad GH (2010) Migration patterns, breeding and moulting locations of king eiders wintering in north-eastern Norway. Polar Biol 33:1379–1385CrossRefGoogle Scholar
  10. Ching HL (1991) Lists of larval worms from marine invertebrates of the Pacific Coast of North America. J Helminthol Soc Wash 58(1):57–68Google Scholar
  11. Chrisanfova GG, Lopatkin AA, Shestak AG, Mishchenkov VA, Zhukova TV, Akimova LN, Semyenova SK (2011) Polymorphism of the cox1 mtDNA gene from cercarial isolates of the avian schistosome Bilharziella polonica (Trematoda: Schistosomatidae) from Belarussian lakes. Russ J Genet 47(5):603–609CrossRefGoogle Scholar
  12. 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, p 78–159 (in Russian)Google Scholar
  13. Combescot-Lang C (1976) Etude des trematodes parasites de Littorina saxatilis (Olivi) et de leurs effets sur cet hote. Ann Parasitol Hum Comp 51:27–36PubMedGoogle Scholar
  14. Crandall KA, Templeon AR (1993) Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 34:959–969Google Scholar
  15. Cribb TH, Bray RA, Olson PD, Timothy D, Littlewood J (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254CrossRefPubMedGoogle Scholar
  16. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772CrossRefPubMedPubMedCentralGoogle Scholar
  17. Dau CP, Flint PL, Petersen MR (2000) Distribution of recoveries of Steller’s Eiders banded on the lower Alaska Peninsula, Alaska. J Field Ornithol 71(3):541–548CrossRefGoogle Scholar
  18. Deblock S (1980) Survey of the larval Trematoda parasites of Hydrobia (Prosobranches) mollusca of the coasts of France. Parassitologia 22(1–2):1–105Google Scholar
  19. Dunton K (1992) Arctic biogeography: the paradox of the marine benthic fauna and flora. Trends Ecol Evol 7(6):183–189CrossRefPubMedGoogle Scholar
  20. Duran S, Gilbert G, Turton X (2004) Phylogeographical history of the sponge Crambe crambe (Porifera, Poecilosclerida): range expansion and recent invasion of the Macaronesian islands from the Mediterranean Sea. Mol Ecol 13:109–122CrossRefPubMedGoogle Scholar
  21. Evans DW, Irwin SWB, Fitzpatrick SM (1997) Metacercarial encystment and in vivo cultivation of Cercaria Zebouri Stunkard 1932 (Digenea: Notocotylidae) to adults identified as Paramonostomum chabaudi Van Strydonck 1965. Int J Parasitol 27(11):1299–1304CrossRefPubMedGoogle Scholar
  22. Evans NA (1985) The influence of environmental temperature upon transmission of the cercariae of Echinostoma liei (Digenea: Echinostomatidae). Parasitology 90(2):269–275CrossRefGoogle Scholar
  23. Evans NA, Gordon DM (1983) Experimental studies on the transmission dynamics of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 87(1):167–174CrossRefGoogle Scholar
  24. Filimonova LV (1971) New species of trematodes of the family Notocotylidae Lühe, 1909 from anseriform birds of Yakutia. In: Theoretical aspects of general helminthology. Nauka, Moscow, p 211–214 (in Russian)Google Scholar
  25. Filimonova LV (1985) Trematodes of the USSR fauna. Notocotylids. Nauka, Moscow (in Russian)Google Scholar
  26. Frame GW (1969) New definitive host, range extension, and notes on the morphology of Tristriata anatis Belopolskaia, 1953 (Trematoda, Notocotylidae) from southeast Alaska. Can J Zool 47(2):265–266CrossRefPubMedGoogle Scholar
  27. Galaktionov KV (1993) Life cycles of trematodes as components of ecosystems. Apatity, Kola Scientific Centre of the Russian Academy of Sciences Publ. 190 pp (in Russian)Google Scholar
  28. Galaktionov KV (2016) Transmission of parasites in the coastal waters of the Arctic seas and the possible effect of climate change. Zoologichesky Zhurnal 95(9):996–1016 (in Russian)Google Scholar
  29. Galaktionov KV, Bustnes JO (1999) Distribution patterns of marine bird digenean larvae in periwinkles along the southern coast of the Barents Sea. Dis Aquat Org 37(3):221–230CrossRefPubMedGoogle Scholar
  30. 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, p 592CrossRefGoogle Scholar
  31. Galaktionov KV, Skírnisson K (2000) Digeneans from intertidal molluscs of SW Iceland. Syst Parasitol 47(2):87–101CrossRefPubMedGoogle Scholar
  32. Galaktionov KV, Blasco-Costa I, Olson PD (2012) Life cycles, molecular phylogeny and historical biogeography of the ‘pygmaeus’ microphallids (Digenea: Microphallidae): widespread parasites of marine and coastal birds in the Holarctic. Parasitology 139:1346–1360CrossRefPubMedGoogle Scholar
  33. Galaktionov KV, Dobrovolskij AA, Podvyaznaya IM (2014) Evolution of morpho-functional organization of trematode parthenogenetic generations. Zoologichesky Zhurnal 93:426–442 (in Russian)Google Scholar
  34. Galaktionov KV, Regel KV, Atrashkevich GI (2010). Microphallus kurilensis sp. nov., a new species of microphallids from the “pygmaeus” species group (Trematoda, Microphallidae) from the coastal areas of Okhotsk and Bering Seas. Parazitologiya 44:496–507 (in Russian)Google Scholar
  35. 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 62:067CrossRefGoogle Scholar
  36. Gérard C, Moné H, Théron A (1993) Schistosoma mansoniBiomphalaria glabrata: dynamics of the sporocyst population in relation to the miracidial dose and host size. Can J Zool 71:1880–1885CrossRefGoogle Scholar
  37. Ginetsinskaya TA (1968) Trematodes, their life cycles, biology and evolution. Leningrad, USSR: Nauka: 410 pp. Translated in 1988 by Amerind Publ. Co. Pvt. Ltd., New Delhi. 559 ppGoogle Scholar
  38. Gonchar A, Galaktionov KV (2016) Substratum preferences in two notocotylid (Digenea, Notocotylidae) cercariae from Hydrobia ventrosa at the White Sea. J Sea Res 113:115–118CrossRefGoogle Scholar
  39. Granovitch A, Johannesson K (2000) Digenetic trematodes in four species of littorina from the West Coast of Sweden. Ophelia 53(1):55–65CrossRefGoogle Scholar
  40. Herber EC (1942) Life history studies on two trematodes of the subfamily Notocotylinae. J Parasitol 28(3):179–196CrossRefGoogle Scholar
  41. Hoberg EP (1992) Congruent and synchronic patterns in biogeography and speciation among seabirds, pinnipeds, and cestodes. J Parasitol 78:601–615CrossRefPubMedGoogle Scholar
  42. Hoberg EP, Adams AM (1992) Phylogeny, historical biogeography, and ecology of Anophryocephalus spp. (Eucestoda: Tetrabothriidae) among pinnipeds of the Holarctic during the late Tertiary and Pleistocene. Can J Zool 70(4):703–719CrossRefGoogle Scholar
  43. Hoberg EP, Adams A (2000) Phylogeny, history and biodiversity: understanding faunal structure and biodiversity in the marine realm. Bull Scand Soc Parasitol 10(2):19–37Google Scholar
  44. James BL (1968) The distribution and keys of species in the family Littorinidae and of their digenean parasites, in the region of Dale, Pembrokeshire. Field Stud 2(5):615–650Google Scholar
  45. James BL (1969) The Digenea of the intertidal prosobranch, Littorina saxatilis (Olivi). J Zool Syst Evol Res 7(1):273–316CrossRefGoogle Scholar
  46. Johnson SR, Herter DR (1990) Bird migration in the Arctic: a review. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 22–43CrossRefGoogle Scholar
  47. Jousson O, Bartoli P (2000) The life cycle of Opecoeloides columbellae (Pagenstecher, 1863) n. comb. (Digenea, Opecoelidae): evidence from molecules and morphology. Int J Parasitol 30:747–760CrossRefPubMedGoogle Scholar
  48. Jouet D, Ferté H, Depaquit J, Rudolfová J, Latour P, Zanella D, Kaltenbach ML, Léger N (2008) Trichobilharzia spp. in natural conditions in Annecy Lake, France. Parasitology Research 103(1):51–58Google Scholar
  49. 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):1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  50. Králová-Hromadová I, Špakulová M, Horáčková E, Turčeková L, Novobilský A, Beck R, Koudela B, Marinculić A, Rajský D, Pybus M (2008) Sequence analysis of ribosomal and mitochondrial genes of the giant liver fluke Fascioloides magna (Trematoda: Fasciolidae): intraspecific variation and differentiation from Fasciola hepatica. J Parasitol 94(1):58–67CrossRefPubMedGoogle Scholar
  51. Kuklin VV (2015) Seabird helminth fauna and parasite life cycles on the Murman Coast of the Barents Sea in winter. Dokl Biol Sci 461(5):612–615Google Scholar
  52. Kulachkova VG (1954) Life cycle and pathogenic importance of the eider trematode Paramonostomum alveatum (Mehlis, 1846). Transactions of General and Theme Conferences of the Zoological Institute of the USSR Academy of Sciences 4:118–122 (in Russian)Google Scholar
  53. Kulachkova VG (1979) Helminths as a cause of common eider’s death in the top of Kandalaksha Bay. In: Uspenskiy SM (ed) Ecology and morphology of eiders in the USSR. Moscow: Nauka, p 19–25 (in Russian)Google Scholar
  54. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874CrossRefPubMedGoogle Scholar
  55. Lauckner G (1980) Diseases of Mollusca: Gastropoda. In: Kinne O (ed) Diseases of marine animals, vol I. Wiley, Chichester, pp 311–424Google Scholar
  56. Leigh JW, Bryant D (2015) Popart: full‐feature software for haplotype network construction. Methods Ecol Evol 6(9):1110–1116CrossRefGoogle Scholar
  57. Leung TLF, Donald KM, Keeney DB, Koehler AV, Peoples RC, Poulin R (2009) Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: life cycles, ecological roles and DNA barcodes. N Z J Mar Freshw Res 43:857–865CrossRefGoogle Scholar
  58. Littlewood DTJ (2006) The evolution of parasitism in flatworms. In: Maule AG, Marks NJ (eds) Parasitic flatworms: molecular biology, biochemistry, immunology and physiology. CAB International, Wallingford, pp 1–36Google Scholar
  59. McCarthy AM (1999) The influence of temperature on the survival and infectivity of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 118(04):383–388CrossRefPubMedGoogle Scholar
  60. McDonald ME (1981) Key to trematodes reported in waterfowl, US Fish and Wildlife Service., p 142Google Scholar
  61. Miura O, Torchin ME, Bermingham E, Jacobs DK, Hechinger RF (2011) Flying shells: historical dispersal of marine snails across Central America. Proc R Soc B P. rspb20111599Google Scholar
  62. Miura O, Torchin ME, Kuris AM, Hechinger RF, Chiba S (2006) Introduced cryptic species of parasites exhibit different invasion pathways. PNAS 103(52):19818–19823CrossRefPubMedPubMedCentralGoogle Scholar
  63. Mollaret I, Jamieson BG, Adlard RD, Hugall A, Lecointre G, Chombard C, Justine JL (1997) Phylogenetic analysis of the Monogenea and their relationships with Digenea and Eucestoda inferred from 28S rDNA sequences. Mol Biochem Parasitol 90(2):433–438CrossRefPubMedGoogle Scholar
  64. Newell CR (1986) The marine fauna and flora of the Isles of Scilly: some marine digeneans from invertebrate hosts. J Nat Hist 20(1):71–77CrossRefGoogle Scholar
  65. Newton I (2003) Geographical patterns in bird migration. In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Berlin, pp 211–224CrossRefGoogle Scholar
  66. Nolan MJ, Cribb TH (2004) The life-cycle of Paracardicoloides yamagutii Martin, 1974 (Digenea: Sainguinicolidae). Folia Parasitol 51:320–326CrossRefPubMedGoogle Scholar
  67. Nolan MJ, Cribb TH (2005) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Adv Parasitol 60:101–163CrossRefPubMedGoogle Scholar
  68. O’Dwyer K, Faltýnková A, Georgieva S, Kosadinova A (2015) An integrative taxonomic investigation of the diversity of digenean parasites infecting the intertidal snail Austrolittorina unifasciata Gray, 1826 (Gastropoda: Littorinidae) in Australia. Parasitol Res 114(6):2381–2397CrossRefPubMedGoogle Scholar
  69. Pearson JC (1972) A phylogeny of life-cycle patterns of the Digenea. Adv Parasitol 10:153–189CrossRefPubMedGoogle Scholar
  70. Petersen MR, Bustnes JO, Systad GH (2006) Breeding and moulting locations and migration patterns of the Atlantic population of Steller’s Eiders Polysticta stelleri as determined from satellite telemetry. J Avian Biol 37(1):58–68CrossRefGoogle Scholar
  71. Pina S, Barandela T, Santos MJ, Russell-Pinto F, Rodrigues P (2009) Identification and description of Bucephalus minimus (Digenea: Bucephalidae) life cycle in Portugal: morphological, histopathological, and molecular data. J Parasitol 95(2):353–359CrossRefPubMedGoogle Scholar
  72. Podlipaev SA (1979) Trematode parthenitae and larvae in the intertidal molluscs of the eastern Murman. In: Poljanskiy GI (ed) Ecological and experimental parasitology, vol. 2. Leningrad University Press, Leningrad, p 47–101 (in Russian)Google Scholar
  73. Prinz K, Kelly TC, O’Riordan RM, Culloty SC (2010) Occurrence of macroparasites in four common intertidal molluscs on the south coast of Ireland. Mar Biodivers Rec 3:e89CrossRefGoogle Scholar
  74. Reid DG (1996) Systematics and evolution of Littorina. The Ray Society, LondonGoogle Scholar
  75. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542CrossRefPubMedPubMedCentralGoogle Scholar
  76. Rothschild M (1938) Notes on the classification of cercariae of the super-family Notocotyloidea (Trematoda), with special reference to the excretory system. Novitates Zoologicae 61(2):75-83.Google Scholar
  77. Sewell RBS (1922) Cercariae indicae. Ind J Med Res Suppl 10:1–360Google Scholar
  78. Skála V, Bulantová J, Walker AJ, Horák P (2014) Insights into the development of Notocotylus attenuatus (Digenea: Notocotylidae) in Lymnaea stagnalis: from mother sporocyst to cercariae. Parasitol Int 63(1):94–99CrossRefPubMedGoogle Scholar
  79. Skírnisson K, Eydal M, Gunnarsson E, Hersteinsson P (1993) Parasites of the arctic fox (Alopex lagopus) in Iceland. J Wildl Dis 29(3):440–446CrossRefPubMedGoogle Scholar
  80. Stunkard HW (1932) Some larval trematodes from the coast in the region of Roscoff, Finistere. Parasitology 24(3):321–343CrossRefGoogle Scholar
  81. Stunkard HW (1970) The marine cercariae of the woods hole Massachusetts region. Biol Bull 138(1):66–76Google Scholar
  82. Stunkard HW (1983) The marine cercariae of the woods hole, Massachusetts region, a review and a revision. Biol Bull 164(2):143–162Google Scholar
  83. Théron A, Moné H, Gérard C (1992) Spatial and energy compromise between host and parasite: the Biomphalaria glabrataSchistosoma mansoni system. Int J Parasitol 22:91–94CrossRefPubMedGoogle Scholar
  84. Théron A, Pages J-R, Rognon A (1997) Schistosoma mansoni: distribution patterns of miracidia among Biomphalaria glabrata snail as related to host susceptibility and sporocyst regulatory processes. Exp Parasitol 85:1–9CrossRefPubMedGoogle Scholar
  85. Thieltges DW, Ferguson MA, Jones CS, Noble LR, Poulin R (2009) Biogeographical patterns of marine larval trematode parasites in two intermediate snail hosts in Europe. J Biogeogr 36(8):1493–1501CrossRefGoogle Scholar
  86. Troitsky SL (1970) The general review of Pleistocene marine faunae at the northern coast of Eurasia. In: Belov NA et al. (eds) The Arctic Ocean and its coasts in Cenozoic. Leningrad: Hydrometeoisdat, p 179–185 (in Russian)Google Scholar
  87. Tsimbaljuk AK, Kulikov VV, Ardasheva NV, Tsimbaljuk EM (1978) Helminths of invertebrates from the intertidal zone of the Iturup island. In: Kusakin OG (ed) Fauna and vegetation of the shelf of the Kuril islands. Moscow: Nauka, p 69–126 (in Russian)Google Scholar
  88. Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds—unraveling migratory connectivity. Trends Ecol Evol 17:76–83CrossRefGoogle Scholar
  89. Werding B (1969) Morphologie, Entwiklung und Ökologie digener Trematoden-Larven der Strandschneke Littorina littorea. Mar Biol 3:306–333CrossRefGoogle Scholar
  90. Zarkhidze VS (1970) The history of development of marine mollusc faunae in the Atlantic sector of Arctic in the late Cenozoic. In: Belov NA et al. (eds) The Arctic Ocean and its coasts in Cenozoic. Leningrad: Hydrometeoisdat, p 186–194 (in Russian)Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Invertebrate ZoologySt Petersburg State UniversitySt PetersburgRussia
  2. 2.Zoological Institute RASSt PetersburgRussia

Personalised recommendations