Digeneans of northern fur seals Callorhinus ursinus (Pinnipedia: Otariidae) from five subpopulations on St. Paul Island, Alaska

Abstract

A parasitological survey of 651 northern fur seals Callorhinus ursinus L. from five subpopulations was conducted on St. Paul Island, Alaska, during July–August 2012–2014. Digenean trematodes were found in 210 of 651 fur seals with a total prevalence of 32.3%. Intensity of infection varied from 1 to 1540 parasites with mean intensity 18.4 ± 111.1 SD and median intensity of 2 specimens per host. Significant differences in prevalence and intensity of infection in northern fur seals between separate rookeries was not observed (Mann–Whitney test; p > 0.05). Four species of digeneans belonging to the families Heterophyidae (Apophallus zalophi Price, 1932, Phocitrema fusiforme Goto and Ozaki, 1930, and Galactosomum ubelakeri (Dailey, 1969)) and Troglotrematidae (Nanophyetus salmincola (Chapin, 1926)) were found. Nanophyetus salmincola is reported from C. ursinus for the first time. We obtained partial 28S rDNA sequences for all digenean species and conducted molecular phylogenetic analysis to demonstrate their phylogenetic relationships.

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

Fig. 1
Fig. 2

References

  1. Bennington E, Pratt I (1960) The life history of the salmon-poisoning fluke, Nanophyetus salmincola (Chapin). J Parasitol 46(1):91–100. https://doi.org/10.2307/3275341

    CAS  Article  PubMed  Google Scholar 

  2. Beuret J, Scott DA, Pearson JC (2000) The cercaria of Galactosomum bearupi Pearson, 1973 (Trematoda: Heterophyidae) at heron and Masthead Islands, Great Barrier Reef, Australia. Syst Parasitol 46(1):69–77. https://doi.org/10.1023/A:1006362921871

    CAS  Article  PubMed  Google Scholar 

  3. Blair D, Tkach VV, Barton DP (2008) Family Troglotrematidae Odhner, 1914. In Bray RA, Gibson DI, Jones A (Eds) Keys to the Trematoda, Volume 3. Wallingford—London: CAB International and The Natural History Museum, pp. 113–142

  4. Bowman DD, Lynn RC (1995) Parasitology for veterinarians, sixth edn. W.B. Saunders Company, Philadelphia

  5. Chapin EA (1926) A new genus and species of trematode, the probable cause of salmon-poisonig in dogs. North Amer Vet 8:36–37

    Google Scholar 

  6. Culurgioni J, D'Amico V, Figus V (2007) Metacercariae of Galactosomum lacteum (Jägerskiöld, 1896) Looss, 1899 (Heterophyidae) from marine teleosts in the Gulf of Cagliari (southern Sardinia, Italy). J Helminthol 81(4):409–413

    Article  PubMed  Google Scholar 

  7. Dailey MD (1969) Stictodora ubelakeri a new species of heterophyid trematode from the California sea lion (Zalophus californianus). Bull South Calif Acad Sci 68:82–85

    Google Scholar 

  8. Dailey MD, Demaree RS, Critchfield RL (2002) Galactosomum stelleri sp. n. (Trematoda: Heterophyidae) from the northern sea-lion, Eumetopias jubatus (Schreber, 1776) (Carnivora: Otariidae). Comp Parasitol 69(1):58–61.

  9. Dailey MD, Brownell RL Jr (1972) A checklist of marine mammal parasites. In: Ridgway SH (ed) Mammals of the sea, biology and medicine, Charles C. Thomas, Springfield, IL

  10. Dailey MD, Hill BL (1970) A survey of metazoan parasites infesting the California (Zalophus californianus) and steller (Eumetopias jubatus) sea lion. Bull South Calif Acad Sci 69:126–132

    Google Scholar 

  11. Dailey MD (2001) Parasitic diseases. In: Dierauf L, Gulland FMD (eds). CRC handbook of marine mammal medicine: health, disease, and rehabilitation, Second Edition, Taylor & Francis Group LLC, DOI: https://doi.org/10.1201/9781420041637.ch18

  12. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(772):8. https://doi.org/10.1038/nmeth.2109

    Google Scholar 

  13. Delyamure SL (1955) Helminthofauna of marine mammals (ecology and phylogeny). Izdatel’stvoAkademiiNauk USSR, Moscow, Russia [In Russian]

    Google Scholar 

  14. Gelatt T, Ream R, Johnson D (2015) Callorhinus ursinus. The IUCN red list of threatened species 2015: e.T3590A45224953. https://doi.org/10.2305/IUCN.UK.2015-4.RLTS.T3590A45224953.en

  15. Gentry RL (2014) Behavior and ecology of the northern fur seal. Princeton University Press, Science

    Google Scholar 

  16. Georgieva S, Selbach C, Faltýnková A, Soldánová M, Sures B, Skírnisson K, Kostadinova A (2013) New cryptic species of the 'revolutum' group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasit Vectors 6:64

  17. Gibson DI (1996) Trematoda. In: Margolis, L. & Kabata, Z. (Eds.), Guide to the parasites of fishes of Canada. Part IV. Canadian Special Publication of Fisheries and Aquatic Sciences, 124

  18. Felix JR (2013) Reported Incidences of Parasitic Infections in Marine Mammals from 1892 to 1978. Zea E-Books Book 20

  19. Ferguson JA, Schreck CB, Chitwood R, Kent ML (2010) Persistence of infection by metacercariae of Apophallus sp., Neascus sp., and Nanophyetus salmincola plus two myxozoans (Myxobolus insidiosus and Myxobolus fryeri) in coho salmon Oncorhynchus kisutch. J Parasitol 96(2):340–347. https://doi.org/10.1645/GE-2289.1

    Article  PubMed  Google Scholar 

  20. Hammer Ǿ, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Paleontol Electron 4:9 http://palaeo-electronica.org/2001_1/past/issue1_01.htm

    Google Scholar 

  21. Hernández-Orts JS, Viola MN, García NA, Crespo EA, González R, García-Varela M, Kuchta R (2015) A checklist of the helminth parasites of marine mammals from Argentina. Zootaxa 20;3936(3):301–334. doi: https://doi.org/10.11646/zootaxa.3936.3.1

  22. Keyes MC (1965) Pathology of the northern fur seal. J Amer Vet Med Assoc 147:1090–1095

    CAS  Google Scholar 

  23. Kuzmina TA, Lisitsyna OI, Lyons ET, Spraker TR, Tolliver SC (2012) Acanthocephalans in northern fur seals (Callorhinus ursinus) and a harbor seal (Phoca vitulina) on St. Paul Island, Alaska: species, prevalence, and biodiversity in four fur seal subpopulations. Parasitol Res 111(3):1049–1058. https://doi.org/10.1007/s00436-012-2930-x

    CAS  Article  PubMed  Google Scholar 

  24. Kuzmina TA, Kuzmin YI, Tkach VV, Spraker TR, Lyons ET (2013) Ecological, morphological, and molecular studies of Acanthocheilonema odendhali (Nematoda: Filarioidea) in northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska. Parasitol Res 112(9):3091–3100. https://doi.org/10.1007/s00436-013-3483-3

    CAS  Article  PubMed  Google Scholar 

  25. Kuzmina TA, Lyons ET, Spraker TR (2014) Anisakids (Nematoda: Anisakidae) from stomachs of northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska: parasitological and pathological analysis. Parasitol Res 113(12):4463–4470. https://doi.org/10.1007/s00436-014-4131-2

    CAS  Article  PubMed  Google Scholar 

  26. Kuzmina TA, Hernández-Orts JS, Lyons ET, Spraker TR, Kornyushyn VV, Kuchta R (2015) Cestode community in northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska. Intl J Parasitol: Parasites and Wildlife 4(2):256–263. https://doi.org/10.1016/j.ijppaw.2015.04.007

    Google Scholar 

  27. Lee OA, Burkanov VN, Neill WH (2014) Population trends of northern fur seals (Callorhinus ursinus) from a metapopulation perspective. J Exp Mar BiolEcol 451:25–34. https://doi.org/10.1016/j.jembe.2013.10.029

    Article  Google Scholar 

  28. Lyons ET (1963) Biology of the hookworm Uncinaria lucasi stiles, 1901, in the northern fur seal Callorhinus ursinus Linn. on the Pribilof Islands, Alaska: PhD dissertation. Colorado State University

  29. 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(3):1397–1400. https://doi.org/10.1007/s00436-012-2881-2

    Article  PubMed  Google Scholar 

  30. MacKenzie K (1987) Parasites as indicators of host populations. Int J Parasitol 17(2):345–352. https://doi.org/10.1016/0020-7519(87)90109-3

    CAS  Article  PubMed  Google Scholar 

  31. Marcogliese DJ (2005) Parasites of the superorganism: are they indicators of ecosystem health? Int J Parasitol 35(7):705–716. https://doi.org/10.1016/j.ijpara.2005.01.015

    Article  PubMed  Google Scholar 

  32. Margolis L, Dailey MD (1972) Revised annotated list of parasites from sea mammals caught off the west coast of North America. NOAA technical report NMFS, SSRF-647:1–23 DOI: https://doi.org/10.5962/bhl.part.23513

  33. Millemann RE, Knapp SE (1970) Biology of Nanophyetus salmincola and “Salmon poisoning” disease. Adv Parasitol 8:1–41. https://doi.org/10.1016/S0065-308X(08)60250-X

    CAS  Article  PubMed  Google Scholar 

  34. 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 Nov. 2010, New Orleans, LA, 1–8

  35. Neiland KA (1961) Suspected role of parasites in non-rookery mortality of fur seals (Callorhinus ursinus). J Parasitol 47(732):5. https://doi.org/10.2307/3275461

    Google Scholar 

  36. Niemi DR, Macy RW (1974) The life cycle and infectivity to man of Apophallus donicus (Skrjabin and Lindtop, 1919) (Trematoda: Heterophyidae) in Oregon. Proc Helminthol Soc Wash 41:223–229

    Google Scholar 

  37. Nyberg PA, Knapp SE, Millemann RE (1967) “Salmon poisoning” disease. IV. Transmission of the disease to dogs by Nanophyetus salmincola eggs. J Parasitol 53(4):694–699. https://doi.org/10.2307/3276754

    CAS  Article  PubMed  Google Scholar 

  38. 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):7. https://doi.org/10.1016/S0020-7519(03)00049-3

    Google Scholar 

  39. Pearson J (1977) A redescription of Galactosomum ubelakeri n. comb. (Digenea: Heterophyidae) from the California sealion, Zalophys californianus. Publicación Especial, Instituto de Biología de la Universidad Nacional Autónoma de México 4:289–294

    Google Scholar 

  40. Pearson J (2008) Family Heterophyidae Leiper, 1909. In Bray RA, Gibson DI, Jones A (Eds) Keys to the Trematoda, Volume 3 Wallingford – London: CAB International and The Natural History Museum, pp. 113–142

  41. Pearson JC, Margolis L, Boyce NP (1978) The metacercaria of Galactosomum phalacrocoracis (Trematoda: Heterophyidae) from pink salmon, Oncorhynchus gorbuscha, from British Columbia waters. Can J Zool 56(10):2235–2238

    Article  Google Scholar 

  42. Price EW (1932) The trematode parasites of marine mammals. Proc US Nat Mus 81(13):1–68. https://doi.org/10.5479/si.00963801.81-2936.1

    Article  Google Scholar 

  43. Rausch R (1953) Studies on the helminth fauna of Alaska. XIII. Disease in the sea otter, with special reference to helminth parasites. Ecology 34(3):584–604. https://doi.org/10.2307/1929729

    Article  Google Scholar 

  44. 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. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  45. Schlegel MW, Knapp SE, Millemann RE (1968) “Salmon poisoning” disease. V. Definitive hosts of the trematode vector, Nanophyetus salmincola. J Parasitol 54(4):770–774. https://doi.org/10.2307/3277038

    CAS  Article  PubMed  Google Scholar 

  46. Sinclair EH, Vlietstra LS, Johnson DS, Zeppelin TK, Byrd GV, Springer AM (2008) Patterns in prey use among fur seals and seabirds in the Pribilof Islands. Deep-Sea Res II 55:1897–1918. https://doi.org/10.1016/j.dsr2.2008.04.031

    Article  Google Scholar 

  47. Skrjabin KI (1952) Trematodes of animals and man. Osnovy Trematodologii. 6. Moscow, Izdatel’stvo AkademiiNauk USSR [in Russian]

  48. Sokolov VE (1998) The northern fur seal: systematic, morphology, ecology, behavior. Nauka, Moscow [in Russian]

    Google Scholar 

  49. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30(9):1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. Stroud RK, Dailey MD (1978) Parasites and associated pathology observed in pinnipeds stranded along the Oregon coast. J Wildl Dis 14(3):292–298. https://doi.org/10.7589/0090-3558-14.3.292

    CAS  Article  PubMed  Google Scholar 

  51. Thaenkham U, Blair D, Nawa Y, Waikagul J (2012) Families Opisthorchiidae and Heterophyidae: are they distinct? Parasitol Int 61:90–93

    CAS  Article  PubMed  Google Scholar 

  52. Thaenkham U, Nawa Y, Blair D, Pakdee W (2011) Confirmation of the paraphyletic relationship between families Opisthorchiidae and Heterophyidae using small and large subunit ribosomal DNA sequences. Parasitol Int 60(4):521–523. https://doi.org/10.1016/j.parint.2011.07.015

    CAS  Article  PubMed  Google Scholar 

  53. Tkach VV, Littlewood DTJ, Olson PD, Kinsella JM, Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56(1):1–15. https://doi.org/10.1023/A:1025546001611

    Article  PubMed  Google Scholar 

  54. Trites AW (1992) Northern fur seals: why have they declined? Aquat Mamm 18(1):3–18

    Google Scholar 

  55. Tyutin AV, Izvekova GI (2013) Infection of mollusks and fish by the trematode Apophallus muehlingi (Jagerskiold, 1898) and its interrelations with intermediate hosts. Inland Water Biol 6(1):52–56

  56. Williams HH, MacKenzie K, McCarthy AM (1992) Parasites as biological indicators of the population biology, migrations, diet, and phylogenetics of fish. Rev Fish Biol Fisher 2:144–176

    Article  Google Scholar 

  57. Yamaguti S (1975) A synoptical review of life histories of digenetic trematodes of vertebrates: with special reference to the morphology of their larval forms. Keigaku Publishing Co, Tikyo

    Google Scholar 

  58. Yoshimura K (1965) On the trematode species Phocitrema fusiforme Goto and Ozaki, 1930 and Cryptocotyle lingua (Creplin, 1825). Jpn J Vet Res 13(2):15–17

    CAS  PubMed  Google Scholar 

  59. Yurakhno MV (1986) Pricetrema callorhini sp. n. (Trematoda, Heterophyidae) a parasite of fur seal. Parazitologia 20:317–320 [In Russian]

    Google Scholar 

  60. Yurakhno MV (1987) Ciureana delamurei sp. n. (Trematoda, Heterophyidae) a parasite of northern fur seal. Parazitologia 21:752–754 [In Russian]

    Google Scholar 

  61. Yurakhno MV (1998) Diseases and parasites. In: Sokolov VE, Aristov AA, Lisitzina TU (eds) The northern fur seal: systematic, morphology, ecology, Behavior. Nauka, Moscow, pp 810–899 [In Russian]

    Google Scholar 

  62. Yurakhnо MV, Taikov IM (1986) Some preliminary results of parasitological dissections of the commander fur seals in 1984–1985. Proceedings of the 9th All-Union Conference “Izuchenie, okhrana i ratsyonal'noe ispol'zovanie morskikh mlekopitajuschikh.” Arkhangelsk, pp 435–436 [In Russian]

Download references

Acknowledgements

The authors thank Dr. Yuriy Kuzmin from the Institute of Zoology NAS of Ukraine for his useful comments and assistance with preparation of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to T. A. Kuzmina.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kuzmina, T.A., Tkach, V.V., Spraker, T.R. et al. Digeneans of northern fur seals Callorhinus ursinus (Pinnipedia: Otariidae) from five subpopulations on St. Paul Island, Alaska. Parasitol Res 117, 1079–1086 (2018). https://doi.org/10.1007/s00436-018-5784-z

Download citation

Keywords

  • Trematoda
  • Heterophyidae
  • Nanophyetus
  • Callorhinus ursinus
  • 28S rDNA sequences
  • Molecular phylogeny