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Polar Biology

, Volume 33, Issue 5, pp 599–606 | Cite as

The prevalence of Toxoplasma gondii in polar bears and their marine mammal prey: evidence for a marine transmission pathway?

  • S. K. Jensen
  • Jon Aars
  • C. Lydersen
  • K. M. Kovacs
  • K. Åsbakk
Original Paper

Abstract

Little is known about the prevalence of the parasite Toxoplasma gondii in the arctic marine food chain of Svalbard, Norway. In this study, plasma samples were analyzed for T. gondii antibodies using a direct agglutination test. Antibody prevalence was 45.6% among polar bears (Ursus maritimus), 18.7% among ringed seals (Pusa hispida) and 66.7% among adult bearded seals (Erignathus barbatus) from Svalbard, but no sign of antibodies were found in bearded seal pups, harbour seals (Phoca vitulina), white whales (Delphinapterus leucas) or narwhals (Monodon monoceros) from the same area. Prevalence was significantly higher in male polar bears (52.3%) compared with females (39.3%), likely due to dietary differences between the sexes. Compared to an earlier study, T. gondii prevalence in polar bears has doubled in the past decade. Consistently, an earlier study on ringed seals did not detect T. gondii. The high recent prevalence in polar bears, ringed seals and bearded seals could be caused by an increase in the number or survivorship of oocysts being transported via the North Atlantic Current to Svalbard from southern latitudes. Warmer water temperatures have led to influxes of temperate marine invertebrate filter-feeders that could be vectors for oocysts and warmer water is also likely to favour higher survivorship of oocycts. However, a more diverse than normal array of migratory birds in the Archipelago recently, as well as a marked increase in cruise-ship and other human traffic are also potential sources of T. gondii.

Keywords

Climate change Disease Arctic 

Notes

Acknowledgments

This study was funded by the Norwegian Polar Institute and performed in collaboration with the Norwegian School of Veterinary Science. The authors thank Heli Routti and Hans Wolkers for providing valuable data, Magnus Andersen and Bjørn Krafft for their help with field collections and the former for constructive comments on the manuscript.

References

  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723CrossRefGoogle Scholar
  2. Andersen M, Hjelset A, Gjertz I, Lydersen C, Gulliksen B (1999) Growth, age at sexual maturity and condition in bearded seals Erignathus barbatus from Svalbard, Norway. Polar Biol 21:179–185CrossRefGoogle Scholar
  3. Andersen SM, Lydersen C, Grahl-Nielsen O, Kovacs KM (2004) Autumn diet of harbour seals Phoca vitulina at Prins Karls Forland, Svalbard assessed via scat and fatty-acid analyses. Can J Zool 82:1230–1245CrossRefGoogle Scholar
  4. Arkush KD, Miller MA, Leutenegger CM, Gardner IA, Packham AE, Heckeroth AR, Tenter AM, Barr BC, Conrad PA (2003) Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels Mytilus galloprovincialis. Int J Parasitol 33:1087–1097CrossRefPubMedGoogle Scholar
  5. Benenson M, Takafuji E, Lemon S, Greenup R, Sulzer A (1982) Oocyst-transmitted toxoplasmosis associated with ingestion of contaminated water. New Engl J Med 307:666–669PubMedCrossRefGoogle Scholar
  6. Berge J, Johnsen G, Nilsen F, Gulliksen B, Slagstad D (2005) Ocean temperature oscillations enable reappearance of blue mussels Mytilus edulis in Svalbard after a 1000 year absence. Mar Ecol Prog Ser 303:167–175CrossRefGoogle Scholar
  7. Bessieres MH, Berrebi A, Cassaing S, Fillaux J, Cambus JP, Berry A, Assouline C, Ayoubi JM, Magnaval JF (2009) Diagnosis of congenital toxoplasmosis: prenatal and neonatal evaluation of methods used in Toulouse University Hospital and incidence of congenital toxoplasmosis. Mem inst Oswaldo Cruz 14(2):388–391Google Scholar
  8. Boltunov A, Belikov S (1999) Beluga Delphinapterus leucas of the Barents, Kara and Laptev Seas. NAMMCO Sci Publ 4:149–168Google Scholar
  9. Brodie P (1971) A reconsideration of aspects of growth, reproduction, and behavior of the white whale Delphinapterus leucas, with reference to the Cumberland Sound, Baffin Island, population. J Fish Res Bd Can 28:1309–1318Google Scholar
  10. Buxton D, Maley S, Wright S, Rodger S, Bartley P, Innes E (2007) Toxoplasma gondii and ovine toxoplasmosis: new aspects of an old story. Vet Parasitol 149:25–28CrossRefPubMedGoogle Scholar
  11. Calvert W, Ramsay MA (1998) Evaluation of age determination of polar bears by counts of cementum growth layer groups. Ursus 10:449–453Google Scholar
  12. Christensen-Dalsgaard SN (2006) Temporal patterns and age structure of polar bears Ursus maritimus in Svalbard, with special emphasis on validation of age determination. MS thesis, University of Tromsø, Tromsø, NorwayGoogle Scholar
  13. Conrad PA, Miller MA, Kreuder C, James ER, Mazet J, Dabritz H, Jessup DA, Gulland F, Grigg ME (2005) Transmission of toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int J Parasitol 35:1155–1168CrossRefPubMedGoogle Scholar
  14. de Moura L, Bahia-Oliveira LM, Wada MY, Jones JL, Tuboi SH, Carmo EH, Ramalho WM, Camargo NJ, Trevisan R, Graça RM, da Silva AJ, Moura I, Dubey JP, Garrett DO (2006) Waterborne toxoplasmosis, Brazil, from field to gene. Emerg Infect Dis 12:326–329PubMedGoogle Scholar
  15. Derocher AE (2005) Population ecology of polar bears at Svalbard, Norway. Popul Ecol 47:267–275CrossRefGoogle Scholar
  16. Derocher AE, Wiig Ø (2002) Postnatal growth in body length and mass of polar bears Ursus maritimus at Svalbard. J Zool 256:343–349CrossRefGoogle Scholar
  17. Derocher AE, Andriashek D, Stirling I (1993) Terrestrial foraging by polar bears during the ice-free period in western Hudson Bay. Arctic 46:251–254Google Scholar
  18. Derocher AE, Wiig Ø, Andersen M (2002) Diet composition of polar bears in Svalbard and the western Barents Sea. Polar Biol 25:448–452Google Scholar
  19. Desmonts G, Remington J (1980) Direct agglutination test for diagnosis of Toxoplasma infection: method for increasing sensitivity and specificity. J Clin Microbiol 11:562–568PubMedGoogle Scholar
  20. Dubey JP, Beattie CP (1988) Toxoplasmosis of animals and man. CRC Press, Boca Raton, FLGoogle Scholar
  21. Dubey JP, Jones JL (2008) Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol 38:1257–1278CrossRefPubMedGoogle Scholar
  22. Dubey JP, Lindsay DS, Speer CA (1998) Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin Microbiol Rev 11:267–299PubMedGoogle Scholar
  23. Dubey JP, Zarnke R, Thomas NJ, Wong SK, Bonn WV, Briggs M, Davis J, Ewing R, Mense M, Kwok OCH, Romand S, Thulliez P (2003) Toxoplasma gondii, Neospora caninum, Sarcocystis neurona, and Sarcocystis canis-like infections in marine mammals. Vet Parasitol 116:275–296CrossRefPubMedGoogle Scholar
  24. Freeman MMR (1973) Polar bear predation on beluga in the Canadian Arctic. Arctic 26:162–163Google Scholar
  25. Frenkel JK, Dubey JP (1973) Effects of freezing on the viability of toxoplasma oocysts. J Parasitol 59:587–588CrossRefPubMedGoogle Scholar
  26. Gajadhar AA, Measures L, Forbes LB, Kaptel C, Dubey JP (2004) Experimental Toxoplasma gondii infection in grey seals (Halichoerus grypus). J Parasitol 90:255–259CrossRefPubMedGoogle Scholar
  27. Hjelset AM, Andersen M, Gjertz I, Lydersen C (1999) Feeding habits of bearded seals Erignathus barbatus from the Svalbard area, Norway. Polar Biol 21:186–193CrossRefGoogle Scholar
  28. Hofman P, Drici MD, Gibelin P, Michiels JF, Thyss A (1993) Prevalence of toxoplasma myocarditis in patients with the acquired immunodeficiency syndrome. Brit Med J 70:376–381Google Scholar
  29. Hulebak KL (1980) Mechanical transmission of larval Trichinella by arctic crustacea. Can J Zoo 58:1388–1390CrossRefGoogle Scholar
  30. Jacobs L, Melton ML (1966) Toxoplasmosis in chickens. J Parasitol 52:1158–1162CrossRefPubMedGoogle Scholar
  31. Johnson CK, Tinker MT, Estes JA, Conrad PA, Staedler M, Miller MA, Jessup DA, Mazet JAK (2009) Prey choice and habitat use drive sea otter pathogen exposure in a resource-limited coastal system. PNAS 106:2242–2247CrossRefPubMedGoogle Scholar
  32. Jones JL, Lopez A, Wilson M, Schulkin J, Gibbs R (2001) Congenital toxoplasmosis: a review. Obstet Gynecol Surv 56:296–305CrossRefPubMedGoogle Scholar
  33. Kniel KE, Lindsay DS, Sumner SS, Hackney CR, Pierson MD, Dubey JP (2002) Examination of attachment and survival of Toxoplasma gondii oocysts on raspberries and blueberries. J Parasitol 88:790–793PubMedGoogle Scholar
  34. Kutz SJ, Elkin B, Gunn A, Dubey JP (2000) Prevalence of Toxoplasma gondii antibodies in muskox Ovibos moschatus sera from northern Canada. J Parasitol 86:879–882PubMedGoogle Scholar
  35. Kutz SJ, Elkin BT, Panayi D, Dubey JP (2001) Prevalence of Toxoplasma gondii antibodies in barren-ground caribou Rangifer tarandus groenlandicus from the Canadian Arctic. J Parasitol 87:439–442PubMedGoogle Scholar
  36. Labansen AL, Lydersen C, Haug T, Kovacs KM (2007) Spring diet of ringed seals Phoca hispida from northwestern Spitsbergen, Norway. ICES J Mar Sci 64:1246–1256Google Scholar
  37. Laidre KL, Heide-Jørgensen MP, Logdson ML, Hobbs RC, Heagerty P, Dietz R, Jørgensen OA, Treble MA (2004) Seasonal narwhal habitat associations in the high Arctic. Mar Biol 145:821–831Google Scholar
  38. Lambourn DM, Jeffries SJ, Dubey JP (2001) Seroprevalence of Toxoplasma gondii in harbor seals Phoca vitulina in southern Puget Sound, Washington. J Parasitol 87:1196–1197PubMedGoogle Scholar
  39. Lindsay DS, Collins MV, Mitchell SM, Cole RA, Flick GJ, Wetch CN, Lindquist A, Dubey JP (2003) Sporulation and survival of Toxoplasma gondii oocysts in seawater. J Eukaryot Microbiol 50:687–688CrossRefPubMedGoogle Scholar
  40. Lindsay DS, Collins MV, Mitchell SM, Wetch CN, Rosypal AC, Flick GJ, Zajac AM, Lindquist A, Dubey JR (2004) Survival of Toxoplasma gondii oocysts Eastern oysters (Crassostrea virginica). J Parasitol 90:1054–1057CrossRefPubMedGoogle Scholar
  41. Lydersen C, Gjertz I (1987) Population parameters of ringed seals (Phoca hispida Schreber, 1775) in the Svalbard area. Can J Zool 65:1021–1027CrossRefGoogle Scholar
  42. Lydersen C, Kovacs KM (2005) Growth and population parameters of the world’s northernmost harbour seals Phoca vitulina residing in Svalbard, Norway. Polar Biol 28:156–163CrossRefGoogle Scholar
  43. Lydersen C, Hammill MO, Kovacs KM (1994) Diving activity in nursing bearded seal Erignathus barbatus pups. Can J Zool 72:96–103CrossRefGoogle Scholar
  44. Lydersen C, Martin AR, Kovacs KM, Gjertz I (2001) Summer and autumn movements of white whales Delphinapterus leucas in Svalbard, Norway. Mar Ecol Prog Ser 219:265–274CrossRefGoogle Scholar
  45. Lydersen C, Martin AR, Gjertz I, Kovacs KM (2007) Satellite tracking and diving behaviour of sub-adult narwhals Monodon monoceros in Svalbard, Norway. Polar Biol 30:437–442CrossRefGoogle Scholar
  46. Matturri L, Quattrone P, Varesi C, Rossi L (1990) Cardiac toxoplasmosis in pathology of acquired immunodeficiency syndrome. Panminerva Med 32:194–196PubMedGoogle Scholar
  47. Mauritzen M, Derocher AE, Wiig O, Belikov SE, Boltunov AN, Hansen E, Garner GW (2002) Using satellite telemetry to define spatial population structure in polar bears in the Norwegian and western Russian Arctic. J Appl Ecol 39:79–90CrossRefGoogle Scholar
  48. Measures LN, Dubey JP, Labelle P, Martineau D (2004) Seroprevalence of Toxoplasma gondii in Canadian pinnipeds. J Wildl Dis 40:294–300PubMedGoogle Scholar
  49. Messier V, Levesque B, Proulx J, Rochette L, Libman M, Ward B, Serhir B, Couillard M, Ogden N, Dewailly E, Hubert B, Déry S, Barthe C, Murphy D, Dixon B (2008) Seroprevalence of Toxoplasma gondii among Nunavik Inuit (Canada). Zoonos Pub Health 56:188–197CrossRefGoogle Scholar
  50. Mikaelian I, Boisclair J, Dubey JP, Kennedy S, Martineau D (2000) Toxoplasmosis in beluga whales Delphinapterus leucas from the St.Lawrence Estuary: two case reports and a serological survey. J Comp Pathol 122:73–76CrossRefPubMedGoogle Scholar
  51. Oksanen A, Tryland M, Johnsen K, Dubey JP (1998) Serosurvey of Toxoplasma gondii in North Atlantic marine mammals by the use of agglutination test employing whole tachyzoites and dithiothreitol. Comp Immunol Microb 21:107–114CrossRefGoogle Scholar
  52. Oksanen A, Åsbakk K, Prestrud KW, Aars J, Derocher AE, Tryland M, Wiig Ø, Dubey JP, Sonne C, Dietz R, Andersen M, Born EW (2009) Prevalence of antibodies against Toxoplasma gondii in polar bears Ursus maritimus from Svalbard and East Greenland. J Parasitol 95:89–94CrossRefPubMedGoogle Scholar
  53. Prestrud KW, Åsbakk K, Fuglei E, Mørk T, Stien A, Ropstad E, Tryland M, Gabrielsen GW, Lydersen C, Kovacs KM, Loonen MJJE, Sagerup K, Oksanen A (2007) Serosurvey for Toxoplasma gondii in arctic foxes and possible sources of infection in the high Arctic of Svalbard. Vet Parasitol 150:6–12CrossRefPubMedGoogle Scholar
  54. Rah H, Chomel BB, Follmann EH, Kasten RW, Hew CH, Farver TB, Garner GW, Amstrup SC (2005) Serosurvey of selected zoonotic agents in polar bears Ursus maritimus. Vet Rec 156:7–13PubMedGoogle Scholar
  55. Reichard MV, Torretti L, Garvon JM, Dubey JP (2008) Prevalence of antibodies to Toxoplasma gondii in wolverines from Nunavut, Canada. J Parasitol 94:764–765PubMedGoogle Scholar
  56. Seaman GA, Lowry LF, Frost KJ (1982) Foods of beluga whales Delphinapterus leucas in western Alaska. Cetology 44:1–19Google Scholar
  57. Smith TG, Sjare B (1990) Predation of belugas and narwhals by polar bears in nearshore areas of the Canadian High Arctic. Arctic 43:99–102Google Scholar
  58. Stempniewicz L (2006) Polar bear predatory behaviour toward moulting barnacle geese and nesting glaucous gulls on Spitsbergen. Arctic 59:247–251Google Scholar
  59. Strøm H (2006) Birds of Svalbard. In: Kovacs KM, Lydersen C (eds) Birds and mammals of Svalbard. Polarhåndbok No. 13. Norwegian Polar Institute, Tromsø, pp 86–191Google Scholar
  60. Tertikski G, Bakken V, Gavrilo M, Krasnov J, Nikolaeva N, Pokrovskaya I (2000) Seabird colony databases of the Barents Sea Region and the Kara Sea. In: Bakken V (ed) The Barents Sea. Norwegian Polar Institute Report Series, Tromsø, Norway, pp 11–34Google Scholar
  61. Thiemann GW, Iverson SJ, Stirling I (2008) Polar bear diets and arctic marine food webs: insights from fatty acid analysis. Ecol Monogr 78:591–613CrossRefGoogle Scholar
  62. Van Pelt RW, Dieterich RA (1973) Staphylococcal infection and toxoplasmosis in a young harbor seal. J Wildlife Dis 9:258–261Google Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • S. K. Jensen
    • 1
    • 2
  • Jon Aars
    • 2
  • C. Lydersen
    • 2
  • K. M. Kovacs
    • 2
  • K. Åsbakk
    • 3
  1. 1.Institute for BiologyUniversity of TromsøTromsöNorway
  2. 2.Norwegian Polar InstituteTromsöNorway
  3. 3.Section of Arctic Veterinary MedicineNorwegian School of Veterinary ScienceTromsöNorway

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