The diversity and ecology of cestodes from the northern fur seals, Callorhinus ursinus (NFS), were examined using newly collected material from 756 humanely harvested subadult males between 2011 and 2014. NFSs were collected from five different haul-outs on St. Paul Island, Alaska. A total of 14,660 tapeworms were collected with a prevalence of 98.5% and intensity up to 107 cestodes per host (mean intensity 19.7 ± 16.5 SD). Three species of tapeworms were found: Adenocephalus pacificus (Diphyllobothriidea) was the most prevalent (prevalence 97.4%), followed by Diplogonoporus tetrapterus (49.7%), and 5 immature specimens of Anophryocephalus cf. ochotensis (Tetrabothriidea) (0.5%). Most of the cestodes found in the NFS were immature (69.7%). However, only 0.9% of cestodes were in larval (plerocercoid) stages. The species composition, prevalence and intensity of cestodes from these NFSs were not statistically different between the five separate haul-outs. Significant increases in the intensity of NFS infections were observed during the study period.

Departamento de Zoología Instituto de Biología Universidad Nacional Autónoma de México Avenida Universidad 3000 Ciudad Universitaria Distrito Federal CP 04510 México ; Institute of Parasitology Biology Centre Czech Academy of Sciences Branišovská 31 České Budějovice 37005 Czech Republic

Department of Microbiology Immunology and Pathology College of Veterinary Medicine and Biomedical Sciences Colorado State University Fort Collins CO 80526 USA

Department of Veterinary Science Gluck Equine Research Center University of Kentucky Lexington KY 40546 0099 USA

Institute of Parasitology Biology Centre Czech Academy of Sciences Branišovská 31 České Budějovice 37005 Czech Republic

Schmalhausen Institute of Zoology NAS of Ukraine vul B Khmelnyts'kogo 15 Kiev 01601 Ukraine

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Afanasyev V.P. Parazitofauna promyslovykh mlekopitajuschikh Komandorskikh ostrovov. Uchenye zapiski LGU. Ser. Biol. 1941;74:93–117. in Russian.

Arsenyev V.A., Zemskij V.A., Studenetskaja I.S. Pischevaja Prom-st'; Moscow: 1973. Marine Mammals. [Morskie Mlekopitajuschie] p. 232. in Russian.

Atrashkevich G. Parasitology in XXI Century – Problems, Methods, Solutions. 2008. Spiny-headed worm genus Corynosoma Lühe, 1904 (Acanthocephala: Polymorphidae) in the Okhotsk sea and parasitic system with dominant species of C. strumosum (Rudolphi, 1819) pp. 38–42. Lema, St. Peterburg; in Russian.

Benson A.J., Trites A.W. Ecological effects of regime shifts in the Bering Sea and eastern North Pacific Ocean. Fish Fish. 2002;3:95–113.

Bowman D.D., Lynn R.C. sixth ed. W.B. Saunders Company; Philadelphia, USA: 1995. Parasitology for Veterinarians; p. 430.

Bush A.D., Lafferty K.D., Lotz J.M., Shostak A.W. Parasitology meets ecology on its own terms: Margolis, revised. J. Parasitol. 1997;84:575–583. PubMed

Bush A.O., Lotz J.M. The ecology of “crowding”. J. Parasitol. 2000;86:212–213. PubMed

Cholodkovsky N.F. Cestodes nouveaux ou peu connus. Troisième série. Ann. Mus. Zool. Acad. Imp. Sci. St. Petrograd. 1914;19:516–523.

Chupakhina T.I. Helminth fauna of the fur seals from Tulenij island. Trudy AtlantNIRO. 1971;39:166–170. in Russian.

Dailey M.D., Brownell R.L.J. A checklist of mammal parasites. In: Ridgeway S.H., Springfield C.C.T., editors. Mammals of the Sea: Biology and Medicine. Thomas; Springfield: 1972. pp. 528–589.

Delyamure S.L. AN USSR; Moscow, Russia: 1955. Helminthofauna of Marine Mammals (Ecology and Phylogeny) p. 518.

Delyamure S.L. Ecological and geographical survey of helmintofauna of the northern fur seal. Helmintologia. 1961;3:73–79. in Russian.

Delyamure S.L., Skrjabin A.S., Serdukov A.M. vol. XI. Nauka; Moscow, Russia: 1985. p. 200. (Essentials of Cestodology. Diphyllobothriata – Flatworm Parasites of Man, Mammals and Birds). in Russian.

Gentry R.L. Princeton University Press; Princeton, NJ: 1998. Behavior and Ecology of the Northern Fur Seal; p. 392.

Halvorsen O., Andersen K. Some effects of population density in infections of Diphyllobothrium dendriticum (Nitzsch) in golden hamster (Mesocricetus auratus Waterhouse) and common gull (Larus canus L.) Parasitology. 1974;69:149–160. PubMed

Hammer Ǿ., Harper D.A.T., Ryan P.D. PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleontol. Electron. 2001;4:9. http://palaeo-electronica.org/2001_1/past/issue1_01.htm

Hernández-Orts J.S., Montero F.E., Juan-García A., García N.A., Crespo E.A., Raga J.A. Intestinal helminth fauna of the South American sea lion Otaria flavescens and fur seal Arctocephalus australis from northern Patagonia, Argentina. J. Helminthol. 2013;87:336–347. PubMed

Hernández-Orts J.S., Scholz T., Brabec J., Kuzmina T., Kuchta R. Unexpected morphological plasticity and global geographical distribution of the Pacific human tapeworm Adenocephalus pacificus (syn. Diphyllobothrium pacificum): molecular and morphological survey. Acta Trop. 2015 (accepted) PubMed

Hoberg E.P. Historical biogeography and modes of speciation across high latitude seas of the Holarctic: concepts for host-parasite coevolution among Phocini (Phocidae) and Tetrabothriidae (Eucestoda) Can. J. Zool. 1995;73:45–57.

Hoberg E.P. Faunal diversity among avian parasite assemblages: the interaction of history, ecology, and biogeography in marine systems. Bull. Scand. Soc. Parasitol. 1996;6:65–89.

Hoberg E.P., Adams A. Phylogeny and historical biogeography and ecology of Anophryocephalus spp. (Eucestoda: Tetrabothriidae) among pinnipeds of the Holarctic during the late Tertiary and Pleistocene. Can. J. Zool. 1992;70:703–719.

Hoberg E.P., Adams A.M. Phylogeny, history and biodiversity: understanding faunal structure and biogeography in the marine realm. Bull. Scand. Soc. Parasitol. 2000;10:19–37.

Hoberg E.P., Galbreath T.O., Cook J.A., Kutz S.J., Polley L. Northern host-parasite assemblages: history and biogeography on the borderlands of episodic climate and environ-mental transition. Adv. Parasitol. 2012;79:1–97. PubMed

Ionita M., Varela M.G., Lyons E.T., Spraker T.R., Tolliver S.C. Hookworms (Uncinaria lucasi) and acanthocephalans (Corynosoma spp. and Bolbosoma spp.) found in dead northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska in 2007. Parasitol. Res. 2008;103:1025–1029. PubMed

Kajimura H. Distribution and migration of northern fur seals (Callorhinus ursinus) in the eastern Pacific. In: Kajimura H., Lander R.H., Perez M.A., York A.E., Bigg M.A., editors. Further Analysis of Pelagic Fur Seal Data Collected by the United States and Canada During 1958–74. NOAA/NMFS/NMML; Seattle: 1980. pp. 4–19.

Kajimura H. 1984. Opportunistic feeding of the northern fur seal, Callorhinus ursinus, in the Eastern North Pacific Ocean and Bering Sea. U.S. Dep. Commer., NOAA Tech. Rep., NMFS SSRF-779, 49 p.

Kamo H. Gendai Kikaku; Tokyo, Japan: 1999. Guide to Identification of Diphyllobothriid Cestodes; p. 146. in Japanese.

Kamo H., Maejima J., Yazaki S., Fukumoto S. Notes on morphology and taxonomy of the genus Diphyllobothrium found from some marine mammals in Japanese environs. J. Yonago Med. Assoc. 1982;33:261–270. in Japanese.

Keyes M.C. US Dep. Inter., US Fish. Wildl. Serv., Mar. Mamm. Biol. Lab.; Seattle, Washington, USA: 1964. Research in Fur Seal Mortality, St. Paul Island, Alaska. 8 July to 24 September 1963; p. 66.

Keyes M.C. Pathology of the northern fur seal. J. Am. Vet. Med. Assoc. 1965;147:1090–1095. PubMed

Kovalenko L.M. vol. 1. Naukova Dumka; Kiev: 1975. Helminth fauna of otariidae inhabiting the Kuril Islands; pp. 137–139. (Marine Mammals: Proceedings of the VI All-Union Council on the study of marine mammals (Kiev, October, 1975)). in Russian.

Krotov A.I., Delyamure S.L. Some aspects of the parasitic worm fauna of mammals and birds of the URSS. Tr. Gelmintol. Lab. 1952;6:278–292. in Russian.

Kuchta R., Caira J.N. Three new species of Echinobothrium (Cestoda: Diphyllidae) from Indo-Pacific stingrays of the genus Pastinachus (Rajiformes: Dasyatidae) Folia Parastiol. 2010;57:185–196. PubMed

Kuchta R., Scholz T., Brabec J., Wicht B. Chapter 17. Diphyllobothrium, Diplogonoporus and Spirometra. In: Xiao L., Ryan U., Feng F., editors. Biology of Foodborne Parasites. Section III Important Foodborne Helminths. CRC Press; Boca Raton, Florida: 2015. pp. 299–326.

Kuzmina T.A., Lisitsyna O.I., Lyons E.T., Spraker T.R., Tolliver S.C. 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. 2012;111:1049–1058. PubMed

Kuzmina T.A., Lyons E.T., Spraker T.R. Anisakids (Nematoda: Anisakidae) from stomachs of northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska: parasitological and pathological analysis. Parasitol. Res. 2014;113:4463–4470. PubMed

Lyons E.T., Spraker T.R., Olson K.D., Tolliver S.C., Bair H.D. Prevalence of hookworms (Uncinaria lucasi Stiles) in northern fur seal (Callorhinus ursinus Linnaeus) pups on St. Paul Island, Alaska, USA: 1986–1999. Comp. Parasitol. 2000;67:218–223.

Lyons E.T., Delong R.L., Spraker T.R., Melin S.R., Tolliver S.C. Observations in 2001 on hookworms (Uncinaria spp.) in otariid pinnipeds. Parasitol. Res. 2003;89:503–505. PubMed

Lyons E.T., Spraker T.R., De Long R.L., Ionita M., Melin S.R., Nadler S.A. Review of research on hookworms (Uncinaria lucasi Stiles, 1901) in northern fur seals (Callorhinus ursinus Linnaeus, 1758) Parasitol. Res. 2011;109:257–265. PubMed

Machida M. Parasites of the northern fur seal and their relationship to the breeding islands. Proc. Jpn. Soc. Syst. Zool. 1969;5:16–17. in Japanese.

Margolis L. Parasitic helminths and arthropods from pinnipedia of the Canadian Pacific coast. J. Fish. Res. Bd. Can. 1956;13:489–505.

Margolis L., Dailey M.D. Revised annotated list of parasites from sea mammals caught off the west coast of North America. Fish. Ser. Rep. 1972;647:1–23.

Markowski S. The cestodes of pinnipeds in the Arctic and other regions. J. Helminthol. 1952;26:171–214.

Nybelin O. Säugetier- und Vogelcestoden von Juan Fernandez. In: Skottsberg C., editor. vol. III. Almqvist & Wiksell; Uppsala, Sweden: 1931. pp. 493–523. (The Natural History of Juan Fernandez and Easter Island, Zoology).

Olsen O.W., Lyons E.T. Life cycle of the hookworm Uncinaria lucasi Stiles of the northern fur seals, Callorhinus ursinus on the Pribilof Islands in the Bering Sea. J. Parasitol. 1962;48(Suppl.):42–43.

Rausch R.L. Studies on the helminth fauna of Alaska. XLI. Observations on cestodes of the genus Diplogonoporus Lönnberg, 1892 (Diphyllobothriidae) Can. J. Zool. 1964;42:1049–1069.

Rausch R.L., Adams A.M., Margolis L. Identity of Diphyllobothrium spp. (Cestoda: Diphyllobothriidae) from sea lions and people along the Pacific coast of South America. J. Parasitol. 2010;96:359–365. PubMed

Ream R. 2008. Northern fur seal research in Alaska, National Marine Mammal Laboratory Alaska Ecosystems Program, Alaska Fisheries Science Center. Quarterly Research Reports, Oct.–Dec. 2008: 1.

Reiczigel J. Confidence intervals for the binomial parameter: some new considerations. Stat. Med. 2003;22:611–621. PubMed

Rózsa L., Reiczigel J., Majoros G. Quantifying parasites in samples of hosts. J. Parasitol. 2000;86:228–232. PubMed

Roberts L.S. The crowding effect revisited. J. Parasitol. 2000;86:209–211. PubMed

Scheffer V.B., Fiscus C.H., Todd E.I. 1984. History of Scientific Study and Management of the Alaskan Fur Seal, Callorhinus ursinus, 1786–1964. NOAA Technical Report NMFS SSRF-780, 70 pp.

Sinclair E.H., Vlietstra L.S., Johnson D.S., Zeppelin T.K., Byrd G.V., Springer A.M. Patterns in prey use among fur seals and seabirds in the Pribilof Islands. Deep-Sea Res. II. 2008;55:1897–1918.

Sokolov V.E., Aristov A.A., Lisitzina T.U., editors. The Northern Fur Seal: Systematic, Morphology, Ecology, Behavior (1998) Nauka; Moscow: 1998. p. 942. in Russian.

Sterling J.T. 2009. Northern fur seal foraging behaviors, food webs, and interactions with oceanographic features in the eastern Bering Sea. PhD Thesis, University of Washington. 209 pp.

Stiles C.W., Hassall A. Internal parasites of the fur seal, Chapter VII. In: Jordan D.S., editor. The Fur Seals and Fur-Seal Islands of the North Pacific Ocean, Part 3. US Government Printing Office; Washington, DC: 1899. pp. 99–177.

Stunkard H.W. Pseudophyllidean cestodes from Alaskan pinnipeds. J. Parasitol. 1948;34:211–228. PubMed

Trites A.W. Northern fur seals: why have they declined? Aquat. Mamm. 1992;18:3–18.

Wardle R.A., McLeod J.A., Stewart I.E. Lühe's “Diphyllobothrium” (Cestoda) J. Parasitol. 1947;33:319–330. PubMed

Yamaguti S. Studies on the helminth fauna of Japan: part 47. Cestodes of marine mammals and birds. Acta Med. Okayama. 1951;7:307–316.

Yurakhno M.V. New species of cestodes Diplogonoporus violettae sp. n., (Cestoda, Diphyllobothriidae), a parasite of Eumetopias jubatus Schreb. from the Bering sea. Parazitologiya. 1986;20:39–45. in Russian.

Yurakhno M.V. Study of the population structure of the northern fur seals. In: Gaevskaja A.V., editor. Parazitologiia i patologiia morskikh organizmov. Tezisy Dokladov IV Vsesojuznogo Simpoziuma, 21–23 April, 1987. USSR; Kaliningrad: 1987. pp. 144–145. Aplantichaskij nauchno-isskedovatelskii institut rybnogo khoziaistva i okeanigrafii. (in Russian.

Yurakhno M.V. Diseases and parasites. In: Sokolov V.E., Aristov A.A., Lisitzina T.U., editors. The Northern Fur Seal: Systematic, Morphology, Ecology, Behavior. Nauka; Moscow, Russia: 1998. pp. 810–899. in Russian.

Yurakhno M.V., Taikov I.M. Study, Protection and Management of Marine Mammals. Proceedings of the 9th All-Union Conference. The Ministry of Fisheries of the USSR; Arkhangelsk: 1986. Some preliminary results of parasitological autopsies of Commander seals in 1984–1985; pp. 435–436. in Russian.

Diphyllobothrium sprakeri n. sp. (Cestoda: Diphyllobothriidae): a hidden broad tapeworm from sea lions off North and South America

Review of metazoan parasites of the northern fur seal (Callorhinus ursinus) and the analysis of the gastrointestinal helminth community of the population on St. Paul Island, Alaska

Broad tapeworms (Diphyllobothriidae), parasites of wildlife and humans: Recent progress and future challenges

Metazoan parasites of California sea lions (Zalophus californianus): A new data and review