Parasitology Research

, Volume 117, Issue 4, pp 1051–1068 | Cite as

Microphallus ochotensis sp. nov. (Digenea, Microphallidae) and relative merits of two-host microphallid life cycles

  • Kirill V. Galaktionov
  • Isabel Blasco-Costa
Original Paper


A new digenean species, Microphallus ochotensis sp. nov., was described from the intestine of Pacific eiders (Somateria mollissima v-nigrum) from the north of the Sea of Okhotsk. It differs from other microphallids in the structure of the metraterm, which consists of two distinct parts: a sac with spicule-like structures and a short muscular duct opening into the genital atrium. Mi. ochotensis forms a monophyletic clade together with other congeneric species in phylograms derived from the 28S and ITS2 rRNA gene. Its dixenous life cycle was elucidated with the use of the same molecular markers. Encysted metacercariae infective for birds develop inside sporocysts in the first intermediate host, an intertidal mollusc Falsicingula kurilensis. The morphology of metacercariae and adults was described with an emphasis on the structure of terminal genitalia. Considering that Falsicingula occurs at the Pacific coast of North America and that the Pacific eider is capable of trans-continental flights, the distribution of Mi. ochotensis might span the Pacific coast of Alaska and Canada. The range of its final hosts may presumably include other benthos-feeding marine ducks as well as shorebirds. We suggest that a broad occurrence of two-host life cycles in microphallids is associated with parasitism in birds migrating along sea coasts. The chances that migrating birds would stop at a site where both first and second intermediate hosts occur are relatively low. The presence of a single molluscan host in the life cycle increases the probability of transmission.


Digenea Microphallidae Trematoda Marine parasites Life cycle Molecular phylogeny Pacific distribution Marine ducks 



We thank Dr. Gennady I. Atrashkevich, Dr. Olga M. Orlovskaja and Kira V. Regel from the Laboratory of Helminthes’ Ecology of the Institute of Biological Problems of the North (Far East Branch of the Russian Academy of Sciences, Magadan), who supplied us with additional material on microphallids from Chukotka and north of the Sea of Okhotsk. We also thank the staff (especially Arina S. Tokmakova) of the Laboratory of Experimental Parasitology of the Herzen State Pedagogical University of Russia (St. Petersburg) for their help with histological treatment of Mi. ochotensis metacercariae. We are grateful to Natalia Lentsman for her help with the translation of the MS into English. We thank the anonymous reviewers for their well-considered comments on an earlier draft of the manuscript.

Funding information

This study was financed by the Russian Foundation for Basic Research (project no. 16-04-00753) and the programmes of the Russian Academy of Sciences “Fundamental Research for the Development of the Russian Arctic Zone” and the Zoological Institute no. АААА-А17-117030310322-3. This research has been partially funded by the Natural History Museum of Geneva.


  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):2523–2530. CrossRefGoogle Scholar
  2. Andreev AV (2005) Important bird areas in the realm of the Sea of Okhotsk. Bull North-East Sci Center, Rus Acad Sci Far East Branch 1:57–77 (in Russian) Google Scholar
  3. Andreev AV (2010) The fall season migration of the Great Knot Calidris tenuirostris over the Sea of Okhotsk coasts. Bull North-East Sci Center, Rus Acad Sci Far East Branch 3:19–28 (in Russian) Google Scholar
  4. Baxter R (1987) Mollusks of Alaska. Shells and Sea Life, Bayside, CaliforniaGoogle Scholar
  5. Bayne CJ, Grevelding CG (2003) Cloning of Schistosoma mansoni sporocysts in vitro and detection of genetic heterogeneity among individuals within clones. J Parasitol 89(5):1056–1060. CrossRefPubMedGoogle Scholar
  6. Belopol’skaya MM (1949) On the organ of irritation in the trematode Spiculotrema litoralis nov. gen. nov. spec. fam Microphallidae Travassos, 1921. CR USSR Acad Sci Moscow (NS) 67:205–208 (in Russian) Google Scholar
  7. Belopol’skaya MM (1952a) Family Microphallidae Travassos, 1920. In: Skrjabin KI (ed) Trematodes of animals and man: fundamentals of trematodology, vol 6. USSR Academy of Sciences Publishing, Moscow, pp 619–756 (in Russian) Google Scholar
  8. Belopol’skaya MM (1952b) Parasite fauna of marine waterfowl. Scientific reports of Leningrad State University (Uchenie Zapiski Leningradskogo Universiteta) 141, ser. Biol 28:127–180 (in Russian) Google Scholar
  9. Belopol’skaya MM (1954) Parasitic fauna of the birds of the Sudszuhinskiy naturel reserve (Primorye). Scientific reports of Leningrad State University (Uchenie Zapiski Leningradskogo Universiteta) 172:3–34 (in Russian) Google Scholar
  10. Belopol’skaya MM (1956) Dependence of shorebirds helminth fauna on migrations. Yearbook Soc Natural Acad Sci Estonian SSR 49:95–104 (in Russian) Google Scholar
  11. Belopol’skaya MM (1963) Family Microphallidae Travassos, 1920. In: Skrjabin KI (ed) Trematodes of animals and man: fundamentals of trematodology, vol 21. USSR Academy of Sciences Publishing, Moscow, pp 259–502 (in Russian) Google Scholar
  12. Belopol’skaya MM (1983) Biology and geography of helminths of migrating birds. In: Poliansky Yu I (ed) Free living and parasitic invertebrates (morphology, biology and evolution) (Trudy biologicheskogo nauchno-issledovatel'skogo instituta Leningradskogo universiteta, vol. 34). Leningrad University Press, Leningrad, pp 174–189 (in Russian) Google Scholar
  13. Biguet J, Deblock S, Capron A (1958) Contribution a la connaissance des Microphallidae Travassos, 1920 (Trematoda). II. Description de deux especes nouvelles du genre Microphallus Ward, 1901 sens. nov. M. debuni et M. canchei, parasites intestinaux des Charadriformes des cotes de France. Considerations sur quelques genres de la sous famille des Microphallidae Ward, 1901 et essai de cle diagnostique des especes du genre Microphallus Ward, 1901. Ann Parasitol Hum Comp 33(4):397–444Google Scholar
  14. Blasco-Costa I, Poulin R (2017) Parasite life-cycle studies: a plea to resurrect an old parasitological tradition. J Helminthol 91(6):647–656. CrossRefPubMedGoogle Scholar
  15. Bridgman JF (1969) Life cycles of Carneophallus choanophallus n. sp. and C. basodactylophallus n. sp. (Trematoda: Microphallidae). Tulane Stud Zool Botany 15:81–104Google Scholar
  16. Bustnes JO, Erikstad KE (1988) The diets of sympatric wintering populations of common eider Somateria mollissima and king eider S. spectabilis in northern Norway. Ornis Fenn 65:163–168Google Scholar
  17. Cable RM, Connor RS, Balling JW (1960) Digenetic trematodes of Puerto Rican shore birds. Sci Surv Porto Rico Virgin Islands 17:187–225Google Scholar
  18. Cantin M, Bedard J, Milne H (1974) The food and feeding of common eiders in the St. Lawrence estuary in summer. Can J Zool 52(3):319–334. CrossRefGoogle Scholar
  19. 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
  20. Deblock S (1971) Contribution à l'étude des Microphallidae Travassos, 1920. XXIV. Tentative de phylogénie et de taxonomie. Bull Mus Hist Nat; 3e sér, 7. Zoologie 7:353–469Google Scholar
  21. Deblock S (1974) Contribution à l'etude des Microphallidae Travassos, 1920 (Trematoda). XXVIII. Microphallus abortivus n. sp. espèceà cycle évolutif abrégé originaire d'Oléron. Ann Parasitol Hum Comp 49(2):175–184. CrossRefGoogle Scholar
  22. Deblock S (1975) Contribution à l'etude des Microphallidae Travassos, 1920 (Trematoda). XXXIII. A propos de onze espèces décrites ou récoltées par P. Oschmarin en Extrême-Orient. Ann Parasitol (Paris) 50(6):715–730Google Scholar
  23. Deblock S (1977) De l'abrégement du cycle évolutif chez les Trématodes Digènes Microphallidés. Excerta Parasitologica en memoria del Dr Eduardo Caballero y Caballero. Instituto de Biologia, publicationes especiales. Mexico 4:151–160Google Scholar
  24. Deblock S (1980) Inventaire des trématodes larvaires parasites des mollusques Hydrobia (Prosobranches) des côtes de France. Parassitologia 22(1–2):1–105PubMedGoogle Scholar
  25. Deblock S (2008) Family Microphallidae Ward, 1901. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol. 3. CABI International and Natural History Museum, London, pp 451–495CrossRefGoogle Scholar
  26. Diaz JI, Cremonte F (2010) Development from metacercaria to adult of a new species of Maritrema (Digenea: Microphallidae) parasitic in the Kelp Gull, Larus dominicanus, from the Patagonian Coast, Argentina. J Parasitol 96(4):740–745. CrossRefPubMedGoogle Scholar
  27. Field LC, Irwin SWB (1999) Digenean larvae in Hydrobia ulvae from Belfast Lough (Northern Ireland) and the Ythan Estuary (north-east Scotland). J Mar Biol Ass UK 79(3):431–435. CrossRefGoogle Scholar
  28. Field LC, Irwin SWB, Saville DH (1998) Use of an in ovo technique to provide adults of Levinseniella sp. No. 17 that were identified as Levinseniella minuta (Trematoda: Microphallidae). J Parasitol 84(4):867–870. CrossRefPubMedGoogle Scholar
  29. Foster N, Feder HM (2002) Biodiversity of Prince William Sound. p. 10-1–10-69. In: Hines AH, Ruiz GM (eds) Biological invasions of cold-water coastal ecosystems: ballast-mediated aIntroductions in Port Valdez / Prince William Sound, Alaska. Final project report, presented to the Regional Citizens’ Advisory Council of Prince William Sound, Valdez, Alaska.
  30. Galaktionov KV (1983) Microphallids of the “pygmaeus” group. I. Description of the species Microphallus pygmaeus (Levinsen, 1881) nec Odhner, 1905 and M. piriformes (Odhner, 1905) nom. nov. (Trematoda: Microphallidae). Vestn Leningr Univ 15:20–30 (in Russian) Google Scholar
  31. Galaktionov KV (1984) Microphallids of the “pygmaeus” group. II. Microphallus triangulatus sp. nov. (Trematoda: Microphallidae). Vestn Leningr Univ 3:5–11 (in Russian) Google Scholar
  32. Galaktionov KV (1988) Cercaria and metacercaria of Levinseniella brachysoma (Trematoda, Microphallidae) from the invertebrates of the White Sea. Parazitologiya 22(4):304–311 (in Russian). Google Scholar
  33. Galaktionov KV (1989) Maritrema murmanica sp. n.—a new microphallid trematode with aberrant life cycle. Parazitologiya 23:412–418 (in Russian). Google Scholar
  34. Galaktionov KV (1991a) The development of the metacercariae of Microphallus pirum (Syn. Levinseniella somateria) (Trematoda: Microphallidae). Parazitologia 25:116–124 (in Russian) Google Scholar
  35. Galaktionov KV (1991b) Some evolutionary tendencies in morphogenesis of the larvae of the hermaphroditic generation of trematodes of the family Microphallidae. Parazitologia 25:520–526 (in Russian) Google Scholar
  36. Galaktionov KV (1993) Life cycles of trematodes as components of ecosystems. Apatity, Kola Scientific Centre of the Russian Academy of Sciences Publ. 190 p (in Russian) Google Scholar
  37. Galaktionov KV (1996) Life cycles and distribution of seabird helminths in the Arctic and sub-Arctic regions. Bull Scand Soc Parasitol 6:31–49Google Scholar
  38. Galaktionov KV (2007) A description of Cercariae falsicingulae I larva nov. (Digenea, Gymnophallidae) parthenogenetic metacercariae and cercariae from Falsicingula gastropods with speculations on the life cycle. Syst Parasitol 68(2):137–146. CrossRefPubMedGoogle Scholar
  39. Galaktionov KV (2017) Patterns and processes influencing helminth parasites of Arctic coastal communities during climate change. J Helminthol 91(04):387–408. CrossRefPubMedGoogle Scholar
  40. Galaktionov KV, Bustnes JO (1999) Distribution patterns of marine bird digenean larvae in periwinkles along the southern Barents Sea coast. Dis Aquat Org 37(3):221–230. CrossRefPubMedGoogle Scholar
  41. Galaktionov KV, Dobrovolskij A (1985) Development and reproduction of the mother generation of parthenitae of trematodes of the genus Microphallus (Plagiorchiida, Microphallidae). Zoologicheskii Zhurnal 64:1468–1475 (in Russian) Google Scholar
  42. 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, 592 p. CrossRefGoogle Scholar
  43. Galaktionov KV, Malkova II (1993) Development of the alimentary tract during morphogenesis of the metacercariae of Levinseniella brachysoma. J Helminthol 67(02):87–94. CrossRefGoogle Scholar
  44. Galaktionov KV, Malkova II (1994) The glands of trematode cercariae of the family Microphallidae Travassos, 1920. Int J Parasitol 24(4):595–604. CrossRefPubMedGoogle Scholar
  45. Galaktionov KV, Malkova II (1995) Changes in the excretory bladder ultrastructure during the morphogenesis of Levinseniella brachysoma (Trematoda: Microphallidae) metacercariae. J Helminthol 69(03):203–212. CrossRefGoogle Scholar
  46. Galaktionov KV, Skírnisson K (2007) New data on Microphallus breviatus Deblock & Maillard, 1975 (Microphallidae: Digenea) with emphasis on the evolution of dixenous life cycles of microphallids. Parasitol Res 100(5):963–971. CrossRefPubMedGoogle Scholar
  47. Galaktionov KV, Malkova II, Irwin SWB, Saville DH, Maguire JG (1996) Developmental changes in the tegument of four microphallid metacercariae in their second (crustacean) intermediate hosts. J Helminthol 70(03):201–210. CrossRefGoogle Scholar
  48. 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
  49. 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(10):1346–1360. CrossRefPubMedGoogle Scholar
  50. 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(12):4587–4593. CrossRefPubMedGoogle Scholar
  51. Gilardoni C, Etchegoin J, Diaz JI, Ituarte C, Cremonte F (2011) A survey of larval digeneans in the commonest intertidal snails from northern Patagonian coast, Argentina. Acta Parasitol 56(2):163. CrossRefGoogle Scholar
  52. Gonchar A, Galaktionov KV (2017) Life cycle and biology of Tristriata anatis (Digenea: Notocotylidae): morphological and molecular approaches. Parasitol Res 116(1):45–59. CrossRefPubMedGoogle Scholar
  53. Grevelding CG (1999) Genomic instability in Schistosoma mansoni. Mol Biochem Parasitol 101(1–2):207–216. CrossRefPubMedGoogle Scholar
  54. 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
  55. Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294(5550):2310–2314. CrossRefPubMedGoogle Scholar
  56. 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
  57. James BL (1969) The Digenea of the intertidal prosobranch, Littorina saxatilis (Olivi). J Zool Syst Evol Res 7(1):273–316. CrossRefGoogle Scholar
  58. Keeney DB, Waters JM, Poulin R (2007) Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Mol Ecol 16(2):431–439. CrossRefPubMedGoogle Scholar
  59. Korsunenko A, Chrisanfova G, Lopatkin A, Beer SA, Voronin M, Ryskov A, Semyenova S (2012) Genetic differentiation of cercariae infrapopulations of the avian schistosome Trichobilharzia szidati based on RAPD markers and mitochondrial cox1 gene. Parasitol Res 110(2):833–841. CrossRefPubMedGoogle Scholar
  60. Kostadinova A, Vaucher C, Gibson DI (2006) Megalophallus deblocki n. sp. (Digenea: Microphallidae) from Rostrhamus sociabilis (Vieillot) (Aves: Accipitridae) in Paraguay. Syst Parasitol 63(2):119–126. CrossRefPubMedGoogle Scholar
  61. Krasnov YV, Shklyarevich GA, Goryaev YI (2009) Feeding habit of the common eider Somateria mollissima in the White Sea. Dokl Biol Sci Jul-Aug 427(1):343–345. CrossRefGoogle Scholar
  62. Krechmar AV, Kondratyev AV (2006). Waterfowl birds of north-east Asia. NESC FEB RAS, Magadan, Russia, 458 p (in Russian) Google Scholar
  63. Kudlai O, Cribb TH, Cutmore SC (2016) A new species of microphallid (Trematoda: Digenea) infecting a novel host family, the Muraenidae, on the northern Great Barrier Reef, Australia. Syst Parasitol 93(9):863–876. CrossRefPubMedGoogle Scholar
  64. Kulikov VV, Tsimbalyuk AK, Baranova TI (1970) Trematodes of invertebrates from the intertidal zone of the Paramushir island. Sci Rep Far East State Univ 16:12–22Google Scholar
  65. Lauckner G (1983) Diseases of Mollusca: Bivalvia. In: Kinne O (ed) Diseases of marine animals, vol 2. Biologische Anstalt Helgoland, Hamburg, pp 477–961Google Scholar
  66. Leung TLF, Poulin R, Keeney DB (2009) Accumulation of diverse parasite genotypes within the bivalve second intermediate host of the digenean Gymnophallus sp. Int J Parasitol 39(3):327–331. CrossRefPubMedGoogle Scholar
  67. Littlewood DTJ, Curini-Galletti M, Herniou EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogen Evol 16:449–466. CrossRefGoogle Scholar
  68. Lockyer AE, Olson PD, Littlewood DTJ (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc 78(2):155–171. CrossRefGoogle Scholar
  69. Madsen JF (1954) On the food habits of diving ducks in Denmark. Dan Rev Game Biol 2:157–266Google Scholar
  70. Miller, MA, Pfeiffer, W, Schwartz, T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, pp. 1–8Google Scholar
  71. Miura O, Kuris AM, Torchin ME, Hechinger RF, Dunham EJ, Chiba S (2005) Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int J Parasitol 35(7):793–801. CrossRefPubMedGoogle Scholar
  72. Montoliu I, Gracenea M, Deblock S (1992) Contribution à l'etude des Microphallidae Travassos, 1920 (Trematoda). XLIV. Peut-on lever l'ambiguité de Microphallus fusiformis Reimer, 1963? Ann Parasitol Hum Comp 67:166–173CrossRefGoogle Scholar
  73. Mulvey M, Aho JM, Lydeard C, Leberg PL, Smith MH (1991) Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 45(7):1628–1640. PubMedGoogle Scholar
  74. Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33(7):733–755. CrossRefPubMedGoogle Scholar
  75. Overstreet RM, Heard RW (1995) A new species of Megalophallus (Digenea: Microphallidae) from the clapper rail, other birds, and the littoral isopod Ligia baudininana. Can J Fish Aquat Sci 52(S1):98–104. CrossRefGoogle Scholar
  76. Petersen MR, Flint DP (2002) Population structure of Pacific Common eiders breeding in Alaska. Condor 104(4):780–787.[0780:PSOPCE]2.0.CO;2Google Scholar
  77. 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):58–68. CrossRefGoogle Scholar
  78. Pois NV, Tsimbalyuk AK, Ardasheva NB (1974) Three new species of marine cercariae from the intertidal zone. Parazitologiya 8(5):413–418 (in Russian) Google Scholar
  79. Poulin R, Cribb TH (2002) Trematode life cycles: short is sweet? Trends Parasitol 18(4):176–183. CrossRefPubMedGoogle Scholar
  80. Prévot G (1974) Recherches sur le cycle biologique et l'ecologie de quelques trematodes nouveaux parasites de Larus argentatus michaellis Naumann dans le Midi de la France. These présentée à la Faculte des Sciences et Techniques de Saint Jérôme pour obtenir le grade de docteur es-sciences. Universite de Droit, d'Economie et des Sciences d'Aix-Marsielle, Marsielle, 319 ppGoogle Scholar
  81. Prévot G, Deblock S (1970) Contribution à l'étude des Microphallidae Travassos, 1920 (Trematoda). XX. Megallophallus carcini n. sp. adulte expérimental d'une métacercaire de Carcinus maenas Pennant. Ann Parasitol Hum Comp 45(2):213–222. CrossRefPubMedGoogle Scholar
  82. Rauch G, Kalbe M, Reusch TBH (2005) How a complex life cycle can improve a parasite’s sex life. J Evol Biol 18(4):1069–1075. CrossRefPubMedGoogle Scholar
  83. Reimer L (1963) Zur Verbreitung der Adulti und Larvenstadien der Familie Microphallidae Viana, 1924, (Trematoda, Digenea) in der Mittleren Ostsee. Z Parasitenkd 23:253–273PubMedGoogle Scholar
  84. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna 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):539–542. CrossRefPubMedPubMedCentralGoogle Scholar
  85. Saville DH, Irwin SWB (1991) In ovo cultivation of Microphallus primas (Trematoda: Microphallidae) metacercariae to ovigerous adults and the establishment of the life-cycle in the laboratory. Parasitology 103(03):479–484. CrossRefPubMedGoogle Scholar
  86. Sela I, Ashkenazy H, Katoh K, Pupko T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res 43(W1):W7–W14. CrossRefPubMedPubMedCentralGoogle Scholar
  87. Smith SJ (1974) Three new microphallid trematodes from Tasmanian birds. Pap Proc R Soc Tasmania 107:197–205Google Scholar
  88. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690. CrossRefPubMedGoogle Scholar
  89. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57(5):758–771. CrossRefPubMedGoogle Scholar
  90. Tamura, K, Peterson, D, Peterson, N, Stecher, G, Nei, M, Kumar, S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739.
  91. Tsimbalyuk AK, Kulikov VV, Baranova TI (1968a) The biology of Microphallus calidris Belopol'skaia et Ryjikov, 1963 (Trematoda : Microphallidae). In: Skryabin KI, Mamaev YL (eds) Helminths of animals of the Pacific Ocean. Nauka, Moscow, pp 125–128 (in Russian) Google Scholar
  92. Tsimbalyuk AK, Kulikov VV, Baranova TI, Tsimbalyuk EM (1968b) Invertebrates from the intertidal of the Bering island—intermediate and additional hosts of helminthes of birds and mammals. In: Skryabin KI, Mamaev YL (eds) Helminths of animals of the Pacific Ocean. Nauka, Moscow, pp 129–151 (in Russian) Google Scholar
  93. Tsimbalyuk AK, Kulikov VV, Ardasheva NV, Tsimbalyuk 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. Nauka, Moscow, pp 69–126 (in Russian) Google Scholar
  94. Webster MS, Marra PP, Haig SM, Bensch S, Holmes RT (2002) Links between worlds—unraveling migratory connectivity. Trends Ecol Evol 17:76–83. CrossRefGoogle Scholar
  95. Werle E, Schneider C, Renner M, Volker M, Fiehn W (1994) Convenient single-step, one tube purification of PCR products for direct sequencing. Nucleic Acids Res 22(20):4354–4355. CrossRefPubMedPubMedCentralGoogle Scholar
  96. Węsławski JM, Stempiewicz L, Galaktionov KV (1994) Summer diet of seabirds from Franz Josef Land archipelago. Polar Res 13(2):173–181. CrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Zoological InstituteRussian Academy of SciencesSt. PetersburgRussia
  2. 2.Department of Invertebrate ZoologySt. Petersburg State UniversitySt. PetersburgRussia
  3. 3.Natural History Museum of GenevaGenevaSwitzerland

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