Advertisement

Polar Biology

, Volume 41, Issue 12, pp 2543–2559 | Cite as

A century of taxonomic uncertainty: re-description of two species of tapeworms (Diphyllobothriidea) from Arctic seals

  • Bjoern C. Schaeffner
  • Oleg Ditrich
  • Roman Kuchta
Original Paper
  • 65 Downloads

Abstract

Diphyllobothriid tapeworms are well-known parasites of mammals including humans. Most species are known for centuries, but the validity of many species and their classification are still poorly understood. Based on new collections and re-observation of museum material, we focus on widely distributed taxa infecting several species of seals (Phocinae) in Arctic and sub-Arctic waters. The existence of two morphologically similar diphyllobothriid species, Diphyllobothrium lanceolatum and Diphyllobothrium schistochilos, is revealed through detailed analyses of morphological and morphometric data as well as supported by genetic data published recently. Both species show a striking similarity in their body shape, which historically resulted in numerous misidentifications and erroneous records in the literature. Despite previous attempts to unequivocally recognize the species identity of these congeners, D. lanceolatum can be differentiated from D. schistochilos by the presence of a triangular scolex with a posterior velum, a rapid maturation of the strobila and the pointed or slightly rounded appearance of the last proglottid. In addition to the re-descriptions of both species, we provide novel information on their host spectrum and biogeographic distribution.

Keywords

Diphyllobothrium lanceolatum Diphyllobothrium schistochilos Cestoda Biogeography Phocidae 

Notes

Acknowledgements

The authors are indebted to T. Tyml (Czech Republic), M.V. Yurakhno (Ukraine), T. Kuzmina (Ukraine) and J. Carie (U.S.A.) who kindly provided material for the present study. We would also like to acknowledge Mrs. Eileen Harris (BMNH), Mrs. Michèle Bruni (MOM), Dr. Sara Brant (MSB), Dr. Helmut Sattmann (NMW), Dr. Phil D. Harris (NMUO), Prof. Dr. Reinhardt Møbjerg Kristensen (SNM), Dr. Anna Phillips (USNM) and Dr. Birger Neuhaus (ZMB) for providing access to the museum collections and the permission to assess material for the present study. Thanks are also due to Daniel Barčák (Slovakia) who provided new sequences of D. lanceolatum. Visits to museum institutions were supported financially by the SYNTHESYS programme of the European Communities (project Nos. DE-TAF-703, DK-TAF-4500, GB-TAF-735 and 926). This study was supported by the Czech Science Foundation (project No. P505/12/G112) and the Institute of Parasitology, Biology Centre of the Czech Academy of Sciences (RVO: 60077344). The authors would also like to thank the Czech Arctic Research Infrastructure “Josef Svoboda Station” (projects CzechPolar2 LM 2015078 and ECOPOLARIS No. CZ.02.1.01/0.0/0.0/16_013/0001708).

Compliance with ethical standards

Conflict of interest

There is no conflict of interest.

Supplementary material

300_2018_2396_MOESM1_ESM.docx (30 kb)
Supplementary material 1 (DOCX 30 kb)
300_2018_2396_MOESM2_ESM.docx (21 kb)
Supplementary material 2 (DOCX 20 kb)

References

  1. Andersen KI (1987) A redescription of Diphyllobothrium stemmacephalum Cobbold, 1858 with comment on other marine species of Diphyllobothrium Cobbold, 1858. J Nat Hist 21:411–427CrossRefGoogle Scholar
  2. Ariola V (1900) Revisione della famiglia Bothriocephalidae s. str. Arch Parasitol 3:369–484Google Scholar
  3. Berta A, Churchill M (2012) Pinniped taxonomy: review of currently recognized species and subspecies, and evidence used for their description. Mamm Rev 42:207–234CrossRefGoogle Scholar
  4. Chervy L (2009) Unified terminology for cestode microtriches: a proposal from the International Workshops on Cestode Systematics in 2002–2008. Folia Parasitol 56:199–230CrossRefGoogle Scholar
  5. Cholodkovsky N (1914) Cestodes nouveaux ou peu connus. Troisième série. Ann Mus Zool Acad Sci Petersb 19:516–523Google Scholar
  6. Dailey MD, Brownell RL (1972) A checklist of marine mammal parasites. In: Ridgway SH (ed) Mammals of the sea: biology and medicine. Charles C. Thomas, Springfield, pp 528–589Google Scholar
  7. Delyamure SL (1955) Helminthofauna of marine mammals (ecology and phylogeny). Akademia Nauk SSSR, Moscow (in Russian) Google Scholar
  8. Delyamure SL, Popov VN (1975) Contribution to the study of the helminth fauna of the bearded seal inhabiting Sakhalin Bay. Nauchnye Doklady Vysshei Skoly Biologicheskiye Nauki 10:7–10 (in Russian) Google Scholar
  9. Delyamure SL, Yurakhno MV, Popov VN (1976) On the helminth fauna of pennipeds form the Karaginsk gulf (The Bering Sea). Parazitologiya 10:325–332 (in Russian) Google Scholar
  10. Delyamure SL, Skryabin AS, Serdiukov AM (1985) Diphyllobothriata – flatworm parasites of man, mammals and birds, vol 9. Nauka USSR, Moscow (in Russian) Google Scholar
  11. Felix JR (2013) Reported incidences of parasitic infections in marine mammals from 1892 to 1978, vol 20. Zea Books, LincolnGoogle Scholar
  12. Fiscus C, Braham H, Krogman B (1976) Distribution and abundance of Bowhead and Beluga whales in the Bering, Chukchi and Beaufort Seas. Environ Assess Alask Cont Shelf 1:273–324Google Scholar
  13. Fulton TL, Strobeck C (2010) Multiple markers and multiple individuals refine true seal phylogeny and bring molecules and morphology back in line. Proc R Soc B 277:1065–1070CrossRefGoogle Scholar
  14. Germanos NK (1895) Bothriocephalus schistochilos n. sp.: Ein neuer Cestode aus dem Darm von Phoca barbata. Jenaischen Z Naturw 30:1–38Google Scholar
  15. Guiart J (1935) Cestodes parasites provenant des campagnes scientifiques du prince Albert I de Monaco. Résult Camp Sci Prince Albert I 91:1–105Google Scholar
  16. Hernández-Orts JS, Scholz T, Brabec J, Kuzmina T, Kuchta R (2015) High morphological plasticity and global geographical distribution of the Pacific broad tapeworm Adenocephalus pacificus (syn. Diphyllobothrium pacificum): molecular and morphological survey. Acta Trop 149:168–178CrossRefGoogle Scholar
  17. Hjelset AM, Andersen M, Gjertz I, Lydersen C, Gulliksen B (1999) Feeding habits of bearded seals (Erignathus barbatus) from the Svalbard area, Norway. Polar Biol 21(3):186–193CrossRefGoogle Scholar
  18. Joyeux C, Baer JG (1936) Faune de France: Cestodes, vol 30. Paul Lechevalier, ParisGoogle Scholar
  19. Kamo H (1999) Guide to identification of diphyllobothriid cestodes. Tokyo, JapanGoogle Scholar
  20. Krabbe H (1865) Helminthologiske Undersøgelser i Danmark og paa Island, med saerligt Hensyn til Blaereormlidelserne paa Island. K Dansk Videnskabernes Selsk Naturvid Math Afhandlinger 7:345–408Google Scholar
  21. Kuchta R, Scholz T (2017) Diphyllobothriidea. In: Caira JN, Jensen K (eds) Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth. University of Kansas, Natural History Museum, Special Publication, Lawrence, pp 167–189Google Scholar
  22. Kuchta R, Scholz T, Brabec J, Narduzzi-Wicht B (2015) Chapter 17 Diphyllobothrium, Diplogonoporus and Spirometra. In: Xiao L, Ryan U, Feng F (eds) Biology of Foodborne Parasites. Section III. Important Foodborne Helminths. CRC Press, Boca Raton, pp 299–326Google Scholar
  23. Kuzmina TA, Hernández-Orts JS, Lyons ET, Spraker TR, Kornyushyn VV, Kuchta R (2015) The cestode community in northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska. Int J Parasitol: Parasit Wildl 4:256–263Google Scholar
  24. Leuckart R (1863) Die menschlichen Parasiten und die von ihnen herrührenden Krankheiten. Ein Hand- und Lehrbuch für Naturforschen und Ärztepp. Leipzig. GermanyGoogle Scholar
  25. Linstow OFB (1878) Neue Beobachtungen an Helminthen. Arch Naturgesch 44:218–245Google Scholar
  26. Linstow OFB (1901) Entozoa des zoologischen Museums der Kaiserlichen Akademie der Wissenschaften zu St. Petersburg I. Bull Acad Sci St Petersb 15:271–292Google Scholar
  27. Linstow OFB (1905a) Helminthen aus Ceylon und aus arktischen Breiten. Z Wiss Zool 82:182–193Google Scholar
  28. Linstow OFB (1905b) Helminthen der russischen Polar-Expedition 1900–1903. Mém Acad Sci St Petersb 18:1–17Google Scholar
  29. Lowry LF, Frost KJ, Burns JJ (1980) Feeding of bearded seals in the Bering and Chukchi Seas and trophic interaction with Pacific walruses. Arctic 33:330–342CrossRefGoogle Scholar
  30. Lühe M (1899) Zur Anatomie und Systematik der Bothriocephaliden. Ver Deutsch Zool Ges 9:30–55Google Scholar
  31. Maltsev VN (1998) On taxonomic status of Diphyllobothrium schistochilus (Cestoda: Pseudophyllidea) – parasite of bearded seal in the Arctic. In: Alimov AF, Galkin AK, Guljajev VD, Dubinina JV (eds) Problemy cestodologii: sbornik nauchnych trudov Vyp 1. Russian Academy of Sciences, St. Petersburg, pp 83–94 (in Russian) Google Scholar
  32. Markowski S (1952) The cestodes of pinnipeds in the Arctic and other regions. J Helminthol 26:171–214CrossRefGoogle Scholar
  33. Overstreet RM (2003) Presidential address: flavor buds and other delights. J Parasitol 89:1093–1107CrossRefGoogle Scholar
  34. Polyanskii YI (1955) The parasitology of fish of northern marine waters of the USSR: parasites of the fish of the Barents Sea. Trudy Zool Inst AN SSSR 19:1–171 (in Russian) Google Scholar
  35. Popov VN (1975) Helminth fauna of Phocidae in the Sea of Okhotsk in fall. Problemy Parazitol 2:116–118 (in Russian) Google Scholar
  36. Popov VN (1982) Helminth fauna of Phoca largha and P. vitulina. In: Polyansky YI (ed) Parazity i parazitozy cheloveka i zhivotnykh. Naukova Dumka, Kiev, pp 153–157 (in Russian) Google Scholar
  37. Rausch RL (2005) Diphyllobothrium fayi n. sp. (Cestoda: Diphyllobothriidae) from the Pacific walrus, Odobenus rosmarus divergens. Comp Parasitol 72:129–135CrossRefGoogle Scholar
  38. Rausch RL, Hilliard DK (1970) Studies on the helminth fauna of Alaska. XLIX. The occurrence of Diphyllobothrium latum (Linnaeus, 1758) (Cestoda: Diphyllobothriidae) in Alaska, with notes on other species. Can J Zool 48:1201–1212CrossRefGoogle Scholar
  39. Rausch RL, Scott EM, Rausch VR (1967) Helminths in eskimos in Western Alaska with particular reference to Diphyllobothrium infection and anaemia. Trans Roy Soc Trop Med Hyg 61:351–357CrossRefGoogle Scholar
  40. Scheel D-M, Slater GJ, Kolokotronis S-O, Potter C, Rotstein D, Tsangaras K, Greenwood A, Helgen KM (2014) Biogeography and taxonomy of extinct and endangered monk seals illuminated by ancient DNA and skull morphology. ZooKeys 409:1–33CrossRefGoogle Scholar
  41. Schmidt-Ries H (1940) Die bisher bei dem kleinen Tümmler (Phocaena phocaena L.) festgestellten Parasiten. Centralbl Bakt Parasitkde 145:89–106Google Scholar
  42. Scholz T, Hanzelová V (1998) Tapeworms of the genus Proteocephalus Weinland, 1858 (Cestoda: Proteocephalidae), parasites of fishes in Europe. Academia, PragueGoogle Scholar
  43. Scholz T, Kuchta R (2016) Fish-borne, zoonotic cestodes (Diphyllobothrium and relatives) in cold climates: a never-ending story of neglected and (re)-emergent parasites. Food Waterborne Parasitol 4:23–38CrossRefGoogle Scholar
  44. Shulman SS (1953) Parazity ryb Belogo morja. AN SSSR, Moscow (in Russian) Google Scholar
  45. Shulman ON, Popov VN (1982) Study of morphological variations in cestode Diphyllobothrium lanceolatus – parasite of bearded seal Thezisy dokladov 8 Vsesoyuznogo sovescheniya. USSR, Astrakhan, pp 412–414 (in Russian) Google Scholar
  46. Spalding MD et al (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583CrossRefGoogle Scholar
  47. Stunkard HW (1948) Pseudophyllidea cestodes from Alaskan pinnipeds. J Parasitol 34:211–228CrossRefGoogle Scholar
  48. Stunkard HW, Schoenborn HW (1936) Notes on the structure, distribution and synonymy of the Diphyllobothrium lanceolatum. Am Mus Novit 880:1–8Google Scholar
  49. Vagin VL (1933) On the helminth fauna of pinnipeds. Trudy Arkt Nauchno-issled Inst 3:51–60 (in Russian) Google Scholar
  50. Waeschenbach A, Brabec J, Scholz T, Littlewood DTJ, Kuchta R (2017) The catholic taste of broad tapeworms – multiple routes to human infection. Int J Parasitol 47:831–843CrossRefGoogle Scholar
  51. Wallach JD (1972) The management and medical care of pinnipeds. J Zoo Anim Med 3:45–72CrossRefGoogle Scholar
  52. Wardle RA, McLeod JA, Stewart IE (1947) Lühe’s “Diphyllobothrium” (Cestoda). J Parasitol 33:319–330CrossRefGoogle Scholar
  53. Wilson DE, Reeder DAM (2005) Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, BaltimoreGoogle Scholar
  54. Yurakhno MV, Maltsev VN (1993) Diphyllobothrium skriabini sp. n. (Cestoda, Diphyllobothriidae), a parasite of Erignathus barbatus Erx. Parazitologiya 27:84–89 (in Russian) Google Scholar
  55. Zschokke F (1903) Die arktischen Cestoden. Fauna Arctica: Eine Zusammenstellung der arktischen Tierformen, mit besonderer Berücksichtigung des Spitzbergen-Gebietes auf Grund der Ergebnisse der deutschen Expedition in das nördliche. Eismeer im Jahre 1898 3:1–32Google Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Institute of Parasitology, Biology CentreCzech Academy of SciencesČeské BudějoviceCzech Republic
  2. 2.Water Research Group, Unit for Environmental Sciences and Management, Potchefstroom CampusNorth-West UniversityPotchefstroomSouth Africa
  3. 3.Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic

Personalised recommendations