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Anisakids (Nematoda: Anisakidae) from stomachs of northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska: parasitological and pathological analysis

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Abstract

Anisakid nematodes parasitize the alimentary tracts of aquatic vertebrates, including northern fur seals (Callorhinus ursinus) (NFS). The main purpose of this study was to estimate the prevalence, intensity, and species composition of anisakids in NFSs on St. Paul Island, Alaska, and to analyze changes in NFS infection with these nematodes during the last decades. The study was carried out on St. Paul Island, Alaska, in July–August 2011–2013. Stomachs of 443 humanely harvested NFS males were collected from five separate haul-out areas. A total of 4,460 anisakid specimens were collected and identified by morphological criteria. Gross and histological examinations of stomachs were also performed. The overall prevalence of NFS infection was 91.2 %; overall mean intensity 10.9, and overall median intensity 6. Five species, Anisakis simplex s. l., Contracaecum osculatum s. l., Pseudoterranova decipiens s. l., P. azarazi and Phocascaris cystophorae, were found. The prevalence of Anisakis was 46.5 %, its intensity 7.5. The prevalence and intensity of Contracaecum, Pseudoterranova, and Phocascaris were 33.6 % and 3.5, 81.9 % and 6.5, and 5.2 % and 1.7, respectively. Significant differences in the prevalence of NFS infection were observed between separate haul-outs. Comparison of the present data with the results of studies performed in the North Pacific in the 1960s, showed a significant decrease in the intensity of NFS infection with anisakids during the last decades. The prevalence of mucosal lesions in NFS stomachs caused by anisakids also decreased from 92 to 20.9 %. Possible reasons for the changes in NFS infection with anisakids are discussed.

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References

  • Adams AM, Murrell KD, Cross JH (1997) Parasites of fish and risks to public health. Rev Sci Technol 16:652–660

    CAS  Google Scholar 

  • Anderson RC (2000) Nematode parasites of vertebrates: their development and transmission, 2nd edn. CABI, Wallingford, Oxon, UK

    Book  Google Scholar 

  • Antonelis GA, Sinclair EH, Ream RR, Robson BW (1997) Inter-island variation in the diet of female northern fur seals (Callorhinus ursinus) in the Bering Sea. J Zool (London) 242:435–451

    Article  Google Scholar 

  • Audicana MT, Ansotegui IJ, de Corres LF, Kennedy MW (2002) Anisakis simplex: dangerous—dead and alive? Trends Parasitol 18:20–25

    Article  PubMed  Google Scholar 

  • Baird FJ, Gasser RB, Jabbar A, Lopata AL (2014) Foodborne anisakiasis and allergy. Mol Cell Probes 28:167–174

    Article  CAS  PubMed  Google Scholar 

  • Baylis HA (1937) On the ascarids parasitic in seals, with special reference to the genus Contracaecum. Parasitology 24:121–130

    Article  Google Scholar 

  • Bowman DD (1995) Parasitology for veterinarians, 6th edn. Saunders, Philadelphia

    Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al., revisited. J Parasitol 83:575–583

    Article  CAS  PubMed  Google Scholar 

  • Choi SC, Lee SY, Song HO, Ryu JS, Ahn MH (2014) Parasitic infections based on 320 clinical samples submitted to Hanyang University, Korea (2004–2011). Korean J Parasitol 52:215–220

    Article  PubMed Central  PubMed  Google Scholar 

  • Dailey MD (1975) The distribution and intraspecific variation of helminth parasites in Pinnipeds. Rappt P-v Réun Comm Int Explor Sci Mer Med 169:338–352

    Google Scholar 

  • Dailey MD and Brownell RL (1972) A checklist of marine mammal parasites. In: Mammals of the Sea. Ed. by S.H. Ridgway. C. Thomas, Springfield, Illinois: 528–589

  • Delyamure SL (1955) Helminthofauna of marine mammals (ecology and phylogeny). Delyamure SL, Skrjabin KI (eds). Moscow, AN USSR, 518 p. [in Russian]

  • Delyamure SL, Skrjabin AS (1960) Helminthofauna of Commandor northern fur seals. Nauchnye Doklady Vysshej Shkoly. Biol Nauk 1960(2):11–14 [in Russian]

    Google Scholar 

  • Delyamure SL, Yurakhno MV, Popov VN (1979) Composition of helminth fauna as indicator of the seal populations. Priroda 5:111–113 [In Russian]

    Google Scholar 

  • Gaevskaya AV (2005) Anisakid nematodes and diseases caused by them in animals and man. EKOSI–Gidrofizika, Sevastopol [In Russian]

    Google Scholar 

  • Hammer Ǿ, Harper DAT, and Ryan PD (2001) PAST: Paleontological Statistics Software Package for Education and Data Analysis. Paleontologia Electronica 4 (1): 9 pp. http://palaeo-electronica.org/2001_1/past/issue1_01.htm

  • 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, WA

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • MacKenzie K (2002) Parasites as biological tags in population studies of marine organisms: an update. Parasitol 124:153–163

    Article  Google Scholar 

  • Marcogliese DJ (2001) Implications of climate change for parasitism of animals in the aquatic environment. Can J Zool 79:1331–1352

    Article  Google Scholar 

  • Mattiucci S, Nascetti G (2008) Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host–parasite co-evolutionary processes. Adv Parasitol 66:47–148

    Article  PubMed  Google Scholar 

  • Mattiucci S, Paggi L, Nascetti G, Ishikura H, Kikuchi K, Sato N, Cianchi R, Bullini L (1998) Allozyme and morphological identification of Anisakis, Contracaecum and Pseudoterranova (Nematoda: Ascaridoidea) from Japanese waters. Syst Parasitol 40:81–92

    Article  Google Scholar 

  • Mattiucci S, Fazii P, De Rosa A, Paoletti M, Megna AS, Glielmo A, De Angelis M, Costa A, Meucci C, Calvaruso V, Sorrentini I, Palma G, Bruschi F, Nascetti G (2013) Anisakiasis and gastroallergic reactions associated with Anisakis pegreffii infection, Italy. Emerg Infect Dis 19:496–499

    Article  PubMed Central  PubMed  Google Scholar 

  • Mattiucci S, Cipriani P, Webb SC, Paoletti M, Marcer F, Bellisario B, Gibson DI, Nascetti G (2014) Genetic and morphological approaches distinguish the three sibling species of the Anisakis simplex species complex, with a species designation as Anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae). J Parasitol 100:199–214

    Article  CAS  PubMed  Google Scholar 

  • McClelland G (2002) The trouble with sealworms (Pseudoterranova decipiens species complex, Nematoda): a review. Parasitol 124:183–203

    Article  Google Scholar 

  • McClelland G, Misra GRK, Martell DJ (1990) Larval anisakine nematodes in various fish species from Sable Island Bank and vicinity. Can Bull Fish Aquat Sci 222:83–113

    Google Scholar 

  • McClelland G, Misra RK, Martell DJ (2000) Spatial and temporal distributions of larval sealworm (Pseudoterranova decipiens, Nematoda: Anisakinae), in Hippoglossoides platessoides (Pleuronectidae) in eastern Canada from 1980 to 1990. ICES J Marine Sci 57:69–88

    Article  Google Scholar 

  • Melin SR, Ream RR, Zeppelin TK (2006) Report of the Alaska Region and Alaska Fisheries Science Center northern fur seal tagging and census workshop, 6–9 September 2005, Alaska Fish Science Center Processed Report 2006–15. NOAA, National Marine Fisheries Service, Seattle

    Google Scholar 

  • Nadler SA, D’Amelio S, Dailey MD, Paggi L, Siu S, Sakanari JA (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from Northern Pacific marine mammals. J Parasitol 91:1413–1429

    Article  CAS  PubMed  Google Scholar 

  • Neiland KA (1961) Role of parasites in non-rookery mortality of fur seals (Callorhinus ursinus). J Parasitol 47(5):732

    Article  Google Scholar 

  • Nieuwenhuizen NE, Lopata AL (2013) Anisakis—a food-borne parasite that triggers allergic host defences. Int J Parasitol 43:1047–1057

    Article  CAS  PubMed  Google Scholar 

  • Nishikawa Y, Tsubokura M, Kato S, Saito Y (2014) Possible anisakiasis associated with fishery resumption. Disaster Med Public Health Prep 3:1–2

    Google Scholar 

  • Olson AC Jr, Lewis MD, Hauser ML (1983) Proper identification of anisakine worms. Am J Med Technol 49(2):111–114

    PubMed  Google Scholar 

  • Paggi L, Mattiucci S, Gibson DI, Berland B, Nascetti G, Cianchi R, Bullini L (2000) Pseudoterranova decipiens species A and B (Nematoda: Ascaridoidea): nomenclatural designation, morphological diagnostic characters and genetic markers. Syst Parasitol 45:185–197

    Article  CAS  PubMed  Google Scholar 

  • Prophet EB, Mills B, Arrington JB, Sobin LH (1992) Armed Forces Institute of Pathology. Laboratory Methods in Histotechnology, 1st edn. American Registry of Pathology, Washington, DC

    Google Scholar 

  • 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

  • Robson BR, Goebel ME, Baker JD, Ream RR, Loughlin TR, Francis RC, Antonelis GA, Costa DP (2004) Separation of foraging habitat among breeding sites of a colonial marine predator, the northern fur seal (Callorhinus ursinus). Can J Zool 82:20–29

    Article  Google Scholar 

  • Scheffer VB, Fiscus CH, Todd EI (1984) History of Scientific Study and Management of the Alaskan Fur Seal, Callorhinus ursinus. NOAA Technical Report NMFS SSRF-780

  • Sinclair EH, Loughlin TR, Pearcy WG (1994) Prey selection by northern fur seals (Callorhinus ursinus) in the eastern Bering Sea. Fishery Bull 92:144–156

    Google Scholar 

  • Sinclair EH, Vlietstra LS, Johnson DS, Zeppelin TK, Byrd GV, Springer AM, Ream RR, JrGL H (2008) Patterns in prey use among fur seals and seabirds in the Pribilof Islands. Deep-Sea Res II 55:1897–1918

    Article  Google Scholar 

  • Skrjabin AC (1960) Helminthofauna of marine mammals in the Pacific and Far Eastern seas: PhD. Thesis Science. Simferopol [In Russian]

  • Skrjabin AS, Popov VN (1981) Using of an index of species diversity in the study of seasonal, age and geographical variation of helminthofauna in pinnipeds. Abstracts of the Symposium of hydroparasitologists at the IV All-Union Congress of the Hydrobiological Society. AS USSR, Institute of Hydrobiology. Kiev:41–42 [In Russian]

  • Skrjabin AS, Yurakhno MV, Popov VN (1982) To the method of using of the helminthological data for differentiation of local populations of marine mammals. In: Study, protection and management of marine mammals, Abstracts of the VIII All-Union Symposium, Astrakhan, 5–8 October, 1982: 332–334 [In Russian]

  • Smith JW (1999) Ascaridoid nematodes and pathology of the alimentary tract and its associated organs in vertebrates, including man: a literature review. Helminthol Abstr 68:49–96

    Google Scholar 

  • Smith JW, Wootten R (1978) Anisakis and Anisakiasis. Adv Parasitol 16:93–163

    Article  CAS  PubMed  Google Scholar 

  • Spraker TR, Lyons ET, Tolliver SC, Bair HD (2003) Ascaridoid nematodes and associated lesions in stomachs of subadult male northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska: (1987–1999). J Vet Diagn Invest 15:432–437

    Article  CAS  PubMed  Google Scholar 

  • Sterling JT (2009) Northern fur seal foraging behaviors, food webs, and interactions with oceanographic features in the eastern Bering Sea. PhD Thesis, University of Washington

  • Sterling JT, Ream RR (2004) At-sea behavior of juvenile male northern fur seals (Callorhinus ursinus). Can J Zool 82:1621–1637

    Article  Google Scholar 

  • Stiles CW, Hassall A (1899) Internal parasites of the fur seal. In: The fur seals and fur seal islands of the North Pacific Ocean (David Starr Jordan Report 1899), part 3. U.S. Treasury Department, Washington, DC, pp 99–177

    Google Scholar 

  • Testa JW (2011) Fur seal investigations, 2008–2009. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-AFSC-226

  • Thompson RM, Mouritsen KN, Poulin R (2005) Importance of parasites and their life cycle characteristics in determining the structure of a large marine food web. J Anim Ecol 74:77–85

    Article  Google Scholar 

  • Timi JT, Paoletti M, Cimmaruta R, Lanfranchi AL, Alarcos AJ, Garbin L, George-Nascimento M, Rodríguez DH, Giardino GV, Mattiucci S (2014) Molecular identification, morphological characterization and new insights into the ecology of larval Pseudoterranova cattani in fishes from the Argentine coast with its differentiation from the Antarctic species, P. decipiens sp. E (Nematoda: Anisakidae). Vet Parasitol 199:59–72

    Article  CAS  PubMed  Google Scholar 

  • Towell RG, Ream RR, York AE (2006) Decline in northern fur seal (Callorhinus ursinus) pup production on the Pribilof Islands. Mar Mam Sci 22(2):486–491

    Article  Google Scholar 

  • Young PC (1972) The relationship between the presence of larval Anisakine nematodes in cod and marine mammals in British home waters. J Appl Ecol 9:459–485

    Article  Google Scholar 

  • 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 [Iin Russian]

    Google Scholar 

  • 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:435–436 [In Russian]

  • Zeppelin TK, Ream RR (2006) Foraging habitats based on the diet of female northern fur seals (Callorhinus ursinus) on the Pribilof Islands, Alaska. J Zool (London) 270:565–576

    Article  Google Scholar 

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Acknowledgments

The investigation (Paper No. 14-14-034) 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 (Institute of Zoology NAS of Ukraine) for his consultations in statistically processing the results, Dr. Yuriy Kuzmin (Institute of Zoology NAS of Ukraine) for his help with image preparation, and Dr. Kerstin Junker (ARC-Onderstepoort Veterinary Institute, South Africa) for her valuable help in editing the manuscript. The images of helminths were made at the Center of Collective use of Scientific Equipment “Animalia” (Institute of Zoology NAS of Ukraine). The authors thank Drs. Michael Williams and Tom Gelatt (NOAA) and the St. Paul Tribal government for allowing collection of stomachs and intestinal tracts from the NFSs and the use of their field laboratory for parasitological studies.

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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 113, 4463–4470 (2014). https://doi.org/10.1007/s00436-014-4131-2

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