Parasitology Research

, Volume 112, Issue 9, pp 3091–3100 | Cite as

Ecological, morphological, and molecular studies of Acanthocheilonema odendhali (Nematoda: Filarioidea) in northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska

  • T. A. Kuzmina
  • Y. I. Kuzmin
  • V. V. Tkach
  • T. R. Spraker
  • E. T. Lyons
Original Paper


Studies of northern fur seal (Callorhinus ursinus Linnaeus, 1758) infection by the filariid nematode Acanthocheilonema odendhali were carried out in 2011–2012 on St. Paul Island, Pribilof Archipelago, Alaska. Skins of 502 humanely harvested northern fur seals from haul-out areas of five rookeries, Polovina (n = 122), Morjovi (n = 54), Zapadni (n = 72), Lukanin (n = 109), and Gorbatch (n = 145), were examined. A. odendhali was found in 18 % of northern fur seals. The prevalence of infection ranged from 12.5 % up to 22.9 % on different haul-out areas on the island. The mean intensity of infection was 1.3 (range 1–7). Detailed morphological examination of collected specimens was performed using light microscopy. Several characters were added to the morphological description of the species, among them lateral thickening of the body cuticle, especially prominent in males, variations in number and position of genital papillae in males, transverse striation of the cuticle, and terminal dilation on tail end in microfilariae. The adult specimens studied had a shorter esophagus than type specimens from the California sea lion described by Perry (1967). Comparison of partial sequences of the mitochondrial cox1 gene from specimens collected from five sampling sites on St. Paul Island and a specimen from the type host and territory in California showed no significant differences and strongly supported conspecificity of the material from Alaska with A. odendhali.



The investigation (Paper No. 13-14-045) is approved by the director of the University of Kentucky Agricultural Experiment Station. The research was done under the authority of the Marine Mammal Protection Act Permit Number 14327 issued to the National Marine Mammal Laboratory.

The authors thank Dr. Igor Dzeverin from the Institute of Zoology NAS of Ukraine for his assistance with statistical analysis the results. The authors also thank Dr. Frances Gulland, Chief Veterinarian from The Marine Mammal Center, Sausalito, California, and to Dr. Greta Karfsur, Colorado State University Diagnostic Laboratory, College of Veterinary Medicine, Fort Collins, Colorado, for collecting Acanthocheilonema specimens from California sea lions and a bearded seal used in molecular studies.

The images of helminthes were made at the Center of collective use of scientific equipment “Animalia” (Institute of Zoology NAS of Ukraine).


  1. Anderson RC (1959) The taxonomy of Dipetalonema spirocauda (Leidy, 1858) = n. comb. (Skrjabinaria spirocauda) and Dirofilaria roemeri (Linstow, 1905) n. comb. (=Dipetalonema roemeri). Can J Zool 37:481–493CrossRefGoogle Scholar
  2. Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission, 2nd edn. CABI, WallingfordCrossRefGoogle Scholar
  3. Anderson RC, Bain O (1976) Keys to the genera of the order Spirurida. Part 3, Diplotriaenoidea, Aproctoidea and Filarioidea. In: Anderson RC, Chabaud AG, Willmott S (eds) CIH keys to the nematode parasites of vertebrates. CABI, Wallingford, pp 59–116Google Scholar
  4. Bain O, Baker M, Chabaud AG (1982) Nouvelles données sur la lignée Dipetalonema. Ann Parasitol (Paris) 57:593–620Google Scholar
  5. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583PubMedCrossRefGoogle Scholar
  6. Chabaud AG, Petter AJ (1961) Remarques sur l'evolution des papilles cloacales chez les nematodes phasmidiens parasites de vertebrés. Parassitologia 3(1–2):51–69Google Scholar
  7. Chabaud AG, Bain O (1976) La lignée Dipetalonema. Nouvel essai de classification. Ann Parasitol Hum Comp 51(3):365–397PubMedGoogle Scholar
  8. Dailey MD, Hill BL (1970) A survey of metazoan parasites infecting the California (Zalophus californianus) and Steller (Eumetopias jubatus) sea lion. Bull South Calif Acad 69:126–132Google Scholar
  9. Dailey MD, Brownell RL (1972) A checklist of marine mammal parasites. In: Ridgway SH (ed) Mammals of the sea. Thomas, Springfield, pp. 528–589Google Scholar
  10. Davis GB, McKenna PB, Kyle MG (1971) Dipetalonema odendhali in a sea lion. N Z Vet J 19(4):78–79PubMedCrossRefGoogle Scholar
  11. Delyamure SL (1955) Helminthofauna of marine mammals (ecology and phylogeny). Delyamure SL, Skrjabin KI (eds). Moscow, AN USSR, 518 p. [in Russian]Google Scholar
  12. Delyamure SL, Dubovoj SZ, Skrjabin AS (1961) The studies of filarias—parasites of fur seals. Izvestija Krymskogo Otdelenija Geograficheskogo obschestva SSSR 6:199–200 [in Russian]Google Scholar
  13. Derycke S, Remerie T, Vierstraete A, Backeljau T, Vanfleteren J (2005) Mitochondrial DNA variation and cryptic speciation within the free-living marine nematode Pellioditis marina. Mar Ecol Prog Ser 300:91–103CrossRefGoogle Scholar
  14. Dunn JL, Wolke RE (1976) Dipetalonerna spirocauda infection in the Atlantic harbor seal (Phoca vitulina concolor). J Wildl Dis 12:531–538PubMedGoogle Scholar
  15. Eley TJ (1981) Dipetalonema spirocauda in Alaskan marine mammals. J Wildl Dis 17:65–67PubMedGoogle Scholar
  16. Forrester DJ, Jackson RF, Miller JF, Townsend BC (1973) Heartworms in captive California sea lions. J Am Vet Med Assoc 163:568–570PubMedGoogle Scholar
  17. Gage LJ (2003) Pinnipedia. In: Fowler ME, Miller RE (eds) Zoo and wild animal medicine, 5th edition. Saunders, Philadelphia pp.459–475Google Scholar
  18. Hammer Ǿ, Harper DAT, Ryan PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleontologia Electronica 4 (1): 9pp.
  19. Hu M, Chilton NB, Zhu XQ, Gasser RB (2002) Single-strand conformation polymorphism-based analysis of mitochondrial cytochrome c oxidase subunit 1 reveals significant substructuring in hookworm populations. Electrophoresis 23:27–34PubMedCrossRefGoogle Scholar
  20. Kagei N, Oda T (1975) Dipetalonema odendhali Perry, 1967 found from Fur Seal, Callorhinus ursinus (Linnaeus, 1758). Bull Inst Publ Health 24(4):203–205 [in Japanese]Google Scholar
  21. Keyes MC (1964) Research in fur seal mortality, St. Paul Island, Alaska. 8 July to 24 September 1963. US Dep Inter, US Fish Wildl Serv, Mar Mamm Biol Lab, Seattle, WashingtonGoogle Scholar
  22. Kovalenko LM (1978) To the fauna of marine mammal parasites of region of Kurilskie Islands. In: Marine Mammals. Proceedings of the 7th All-Union Conference on Marine Mammal study. Moscow: 154–156 [In Russian]Google Scholar
  23. Leidernberger S, Boström S (2008) Characterization of the heartworm Acanthocheilonema spirocauda (Leidy, 1858) Anderson, 1992 (Nematoda: Onchocercidae) in Scandinavia. Parasitol Res 104:63–67CrossRefGoogle Scholar
  24. Lyons ET, Kuzmina TA, Tolliver SC, Spraker TR (2012) Update on the prevalence of the hookworm, Uncinaria lucasi, in northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska, 2011. Parasitol Res 111:1397–1400PubMedCrossRefGoogle Scholar
  25. Macdonald DW, Gilchrist EW (1969) Dipetalonema spirocauda and Pseudomonas aeruginosa infection in a harbor seal. Can Vet J 10:220–221PubMedGoogle Scholar
  26. Machida M (1977) Two species of Dipetalonema from pinnipeds caught off northern Japan. Bull Nat Sci Mus Tokyo Ser A Zool 3(2):67–71Google Scholar
  27. Measures LN, Gosselin JF, Bergeron E (1997) Heartworm, Acanthocheilonema spirocauda (Leidy, 1858), infections in Canadian phocid seals. Can J Fish Aquat Sci 54:842–846Google Scholar
  28. Nikolskij OR (1969) On the parasite fauna of fur seals in pelagic period of their life. In: Problemy Parazitologii. Proceedings of the 6th Scientific Conference of Parasitologists of the USSR, part 1, Kiev, Naukova Dumka: 179–184 [In Russian]Google Scholar
  29. NWAFC Processed Report 79-1 (1979) Fur seal Investigations, 1978. Northwest and Alaska Fisheries Center, National Marine Fisheries Service, U.S. Department of Commerce. NOAA, Seattle, WashingtonGoogle Scholar
  30. NWAFC Processed Report 81-2 (1981) Fur Seal Investigations, 1980. National Marine Mammal Laboratory, Northwest and Alaska Fisheries Center, National Marine Fisheries Service, NOAA, Seattle, WashingtonGoogle Scholar
  31. Papadopoulos E, Loukopoulos P, Komnenou A, Androukaki E, Karamanlidis A (2010) First report of Acanthocheilonema spirocauda in the Mediterranean monk seal (Monachus monachus). J Wild Dis 46(2):570–573Google Scholar
  32. Perry ML (1967) A new species of Dipetalonema from the California sea lion and a report of Microfilariae from a Steller sea lion (Nematoda: Filarioidea). J Parasitol 53(5):1076–1081PubMedCrossRefGoogle Scholar
  33. Perry ML, Forrester DJ (1971) Dipetalonema odendhali (Nematoda: Filarioidea) from the northern fur seal, with a description of the microfilaria. J Parasitol 57(3):469–472PubMedCrossRefGoogle Scholar
  34. Shults LM (1982) Helminths of the spotted seal, Phoca largha, from the Bering Sea. J Wild Dis 18(1):59–62Google Scholar
  35. Sonin MD (1975) Filariata of animals and man and diseases caused by them. In the: Essentials of Nemathology. Vol. XXIV, part 3. Filariidae, Onchocercinae. Moscow: Nauka [In Russian]Google Scholar
  36. Stroud RK, Dailey MD (1978) Parasites and associated pathology observed in pinnipeds stranded along the Oregon coast. J Wildl Dis 14:292–298PubMedGoogle Scholar
  37. Testa JW (ed) (2011) Fur seal investigations, 2008–2009. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-AFSC-226Google Scholar
  38. Tkach V, Pawlowski J (1999) A new method of DNA extraction from the ethanol-fixed parasitic worms. Acta Parasitol 44:147–148Google Scholar
  39. Uni S, Bain O, Suzuki K, Agatsuma T, Harada M, Motokawa M, Martin C, Lefoulon E, Fukuda M, Takaoka H (2012) Acanthocheilonema delicata n. sp. (Nematoda: Filarioidea) from Japanese badgers (Meles anakuma): description, molecular identification, and Wolbachia screening. Parasit Int 62:14–23CrossRefGoogle Scholar
  40. Yurakhno MV (1998) Diseases and parasites. In: Sokolov VE, Aristov AA, Lisitzina TU (eds) The northern fur seal. Systematic, morphology, ecology, behavior. Nauka, Moscow: 810–899 [in Russian]Google Scholar
  41. Yurakhno MV (2004) About originality of helminthes in pinnipeds. In: Belkovich VM (ed) Marine mammals of the holarctic. KMK, Moscow, pp. 597–599Google Scholar
  42. Yurakhno MV, Taikov IM (1986) Some preliminary results of parasitological autopsies of Commander seals in 1984–1985. In: Study, protection and management of marine mammals. Proceedings of the 9th All-Union Conference, Arkhangelsk: 435–436Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • T. A. Kuzmina
    • 1
  • Y. I. Kuzmin
    • 1
  • V. V. Tkach
    • 2
  • T. R. Spraker
    • 3
  • E. T. Lyons
    • 4
  1. 1.Schmalhausen Institute of Zoology NAS of UkraineKyivUkraine
  2. 2.Department of BiologyUniversity of North DakotaGrand ForksUSA
  3. 3.Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical SciencesColorado State UniversityFort CollinsUSA
  4. 4.Department of Veterinary ScienceUniversity of Kentucky, Gluck Equine Research CenterLexingtonUSA

Personalised recommendations