Pathogen surveillance in Southern Ocean pinnipeds

  • Sandra Núñez-Egido Department of Arctic and Marine Biology, UiT The Arctic University of Norway, Tromsø, Norway
  • Andrew Lowther Norwegian Polar Institute, Fram Centre, Tromsø, Norway
  • Ingebjørg H. Nymo Norwegian Veterinary Institute, Tromsø, Norway
  • Jörn Klein Department of Nursing and Health Sciences, University of South-Eastern Norway, Kongsberg, Norway
  • Eva M. Breines Department of Arctic and Marine Biology, UiT The Arctic University of Norway, Tromsø, Norway
  • Morten Tryland Department of Arctic and Marine Biology, UiT The Arctic University of Norway, Tromsø, Norway; and Norwegian Polar Institute, Fram Centre, Tromsø, Norway
Keywords: Antarctic fur seal, parapoxvirus, Southern elephant seal, Southern Ocean, wildlife disease, zoonosis


Knowledge of the health status and potential effect of disease outbreaks among Southern Ocean fauna may be decisive for its conservation. We assessed the exposure and infection of Antarctic fur seals (Arctocephalus gazella, AFS) and Southern elephant seals (Mirounga leonine, SES) to parapoxvirus, Phocid alphaherpesvirus-1 (PhHV-1), smooth Brucella spp. and Toxoplasma gondii. AFS (n = 65) serum and swab samples, and SES (n = 13) serum samples from the sub--Antarctic island of Bouvetøya (54°25’S, 03°22’E) were collected during two austral summers (2014/15, 2017/18). Three polymerase chain reaction (PCR) tests amplifying the DNA polymerase, B2L and GIF parapoxvirus genomic regions were performed, investigating DNA from mucosal swab samples. The glycoprotein B gene was targeted to detect PhHV-1 viral DNA. Sera were assayed for T. gondii and smooth Brucella spp. antibodies with indirect enzyme-linked immunosorbent assays. Parapoxvirus PCR amplicons of the expected size were generated in two of the 29 AFS pups (nasal swabs, 2014/15), targeting the B2L (n = 2) and DNA polymerase (n = 1) genes, whereas the GIF PCR did not amplify target sequences. The PCR amplicons were sequenced and blasted in GenBank, revealing highest similarity with a seal parapoxvirus, confirming the presence of the virus in AFS for the first time. No PhHV-1 amplicons were generated, and antibodies against T. gondii or smooth Brucella spp. were not detected. Our data indicate that these seals are host for parapoxvirus but are neither exposed to smooth Brucella spp. nor T. gondii. Evidence of PhHV-1 shedding was not detected.


Download data is not yet available.


Abalos P., Retamal P., Blank O., Torres D. & Valdenegro V. 2009. Brucella infection in marine mammals in Antarctica. Veterinary Record 164, 346–346, doi: 10.1136/vr.164.8.250.

Arthur B., Hindell M., Bester M., De Bruyn P.N., Trathan P., Goebel M. & Lea M.A. 2017. Winter habitat predictions of a key Southern Ocean predator, the Antarctic fur seal (-Arctocephalus gazella). Deep-Sea Research Part II 140, 171–181, doi: 10.1016/j.dsr2.2016.10.009.

Becher P., König M., Müller G., Siebert U. & Thiel H.J. 2002. Characterization of sealpox virus, a separate member of the parapoxviruses. Archives of Virology 147, 1133–1140, doi: 10.1007/s00705-002-0804-8.

Blanchet M.A., Godfroid J., Breines E.M., Heide-Jørgensen M.P., Nielsen N.H., Hasselmeier I., Iversen M., Jensen S.K. & Åsbakk K. 2014. West Greenland harbour porpoises assayed for antibodies against Toxoplasma gondii: false positives with the direct agglutination method. Diseases of Aquatic Organisms 108, 181–186, doi: 10.3354/dao02715.

Borst G.H.A., Walvoort H.C., Reijnders P.J.H., Van Der Kamp J.S. & Osterhaus A.D.M.E. 1986. An outbreak of a herpesvirus infection in harbor seals (Phoca vitulina). Journal of Wildlife Diseases 22, 1–6, doi: 10.7589/0090-3558-22.1.1.

Bossart G.D. 2011. Marine mammals as sentinel species for oceans and human health. Veterinary Pathology 48, 676–690, doi: 10.1177/0300985810388525.

Boyd I.L., Staniland I.J. & Martin A.R. 2002. Distribution of foraging by female Antarctic fur seals. Marine Ecology Progress Series 242, 285–294, doi: 10.3354/meps242285.

Bracht A.J., Brudek R.L., Ewing R.Y., Manire C.A., Burek K.A., Rosa C., Beckmen K.B., Maruniak J.E. & Romero C.H. 2006. Genetic identification of novel poxviruses of cetaceans and pinnipeds. Archives of Virology 151, 423–438, doi: 10.1007/s00705-005-0679-6.

Burek K.A., Gulland F.M. & O’Hara T.M. 2008. Effects of climate change on Arctic marine mammal health. Ecological Applications 18, 126–134, doi: 10.1890/06-0553.1.

Clark C., McIntyre P.G., Evans A., McInnes C.J. & Lewis‐Jones S. 2005. Human sealpox resulting from a seal bite: confirmation that sealpox virus is zoonotic. British Journal of Dermatology 152, 791–793, doi: 10.1111/j.1365-2133.2005.06451.x.

Crane A., Goebel M.E., Kraberger S., Stone A.C. & Varsani A. 2018. Novel anelloviruses identified in buccal swabs of Antarctic fur seals. Virus Genes 54, 719–723, doi: 10.1007/s11262-018-1585-9.

Daszak P., Cunningham A.A. & Hyatt A.D. 2000. Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 287, 443–449, doi: 10.1126/science.287.5452.443.

Daszak P., Cunningham A.A. & Hyatt A.D. 2001. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78, 103–116, doi: 10.1016/S0001-706X(00)00179-0.

Desforges J.P.W., Sonne C., Levin M., Siebert U., De Guise S. & Dietz R. 2016. Immunotoxic effects of environmental pollutants in marine mammals. Environment International 86, 126–139, doi: 10.1016/j.envint.2015.10.007.

Edwards D.D., McFeters G.A. & Venkatesan M.I. 1998. Distribution of Clostridium perfringens and fecal sterols in a benthic coastal marine environment influenced by the sewage outfall from McMurdo Station, Antarctica. Applied and Environmental Microbiology 64, 2596–2600, doi: 10.1128/AEM.64.7.2596-2600.1998.

Eisenberg T., Hamann H.P., Kaim U., Schlez K., Seeger H., Schauerte N., Melzer F., Tomaso H., Scholoz H.C., Koylass M.S., Whatmore A.M. & Zschöck M. 2012. Isolation of potentially novel Brucella spp. from frogs. Applied and Environmental Microbiology 78, 3753–3755, doi: 10.1128/AEM.07509-11.

Felsenstein J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791, doi: 10.1111/j.1558-5646.1985.tb00420.x.

Frenot Y., Chown S.L., Whinam J., Selkirk P.M., Convey P., Skotnicki M. & Bergstrom D.M. 2005. Biological invasions in the Antarctic: extent, impacts and implications. Biological Reviews 80, 45–72, doi: 10.1017/S1464793104006542.

Frey H.R., Liess B., Haas L., Lehmann H. & Marschall H.J. 1989. Herpesvirus in harbour seals (Phoca vitulina): isolation, partial characterization and distribution. Journal of Veterinary Medicine Series B 36, 699–708, doi: 10.1111/j.1439-0450.1989.tb00664.x.

García-Peña F.J., Pérez-Boto D., Jiménez C., San Miguel E., Echeita A., Rengifo-Herrera C., García-Párraga D., Ortega-Mora L.M. & Pedraza-Díaz S. 2010. Isolation and characterization of Campylobacter spp. from Antarctic fur seals (Arctocephalus gazella) at Deception Island, Antarctica. Applied Environmental Microbiology 76, 6013–6016, doi: 10.1128/AEM.00316-10.

Godfroid J. 2002. Brucellosis in wildlife. Revue Scientifique et Technique-Office International des Épizooties 21, 277–286, doi: 10.20506/rst.21.2.1333.

Goldstein T., Mazet J.A., Gulland F.M., Rowles T., Harvey J.T., Allen S.G., King D.P., Aldridge B.M. & Stott J.L. 2004. The transmission of phocine herpesvirus-1 in rehabilitating and free-ranging Pacific harbor seals (Phoca vitulina) in California. Veterinary Microbiology 103, 131–141, doi: 10.1016/j.vetmic.2004.06.017.

Goldstein T., Zabka T.S., Delong R.L., Wheeler E.A., Ylitalo G., Bargu S., Silver M., Leighfield T., Van Dolah F., Langlois G., Sidor I., Dunn J.L. & Gulland F.M. 2009. The role of domoic acid in abortion and premature parturition of California sea lions (Zalophus californianus) on San Miguel Island, California. Journal of Wildlife Diseases 45, 91–108, doi: 10.7589/0090-3558-45.1.91.

Gulland F.M.D., Lowenstine L.J., Lapointe J.M., Spraker T. & King D.P. 1997. Herpesvirus infection in stranded Pacific harbor seals of coastal California. Journal of Wildlife Diseases 33, 450–458, doi: 10.7589/0090-3558-33.3.450.

Günther T., Haas L., Alawi M., Wohlsein P., Marks J., Grundhoff A., Becher P. & Fischer N. 2017. Recovery of the first full-length genome sequence of a parapoxvirus directly from a clinical sample. Scientific Reports 7, article no. 3734, doi: 10.1038/s41598-017-03997-y.

Harder T.C, Plötz J. & Liess B. 1991. Antibodies against European phocine herpesvirus isolates detected in sera of Antarctic seals. Polar Biology 11, 509–512, doi: 10.1007/BF00233087.

Harvell C.D., Kim K., Burkholder J.M., Colwell R.R., Epstein P.R, Grimes D.J, Hofmann E.E, Lipp E.K., Osterhaus A.D.M.E., Overstreet R.M., Porter J.W, Smith GW & Vasta G.R. 1999. Emerging marine diseases-climate links and anthropogenic factors. Science 285, 1505–1510, doi: 10.1126/science.285.5433.1505.

Hernández J., Prado V., Torres D., Waldenström J., Haemig P.D. & Olsen B. 2007. Enteropathogenic Escherichia coli (EPEC) in Antarctic fur seals Arctocephalus gazella. Polar Biology 30, 1227–122, doi: 10.1007/s00300-007-0282-2.

Hicks B.D, & Worthy G.A. 1987. Sealpox in captive grey seals (Halichoerus grypus) and their handlers. Journal of Wildlife Disease 23, 1–6, doi: 10.7589/0090-3558-23.1.1.

Hindell M.A., McMahon C.R., Bester M.N., Boehme L., Costa D., Fedak M.A, Guinet C., Herraiz‐Borreguero L., Harcourt R.G., Huckstadt L., Kovacs K.M., Lydersen C., McIntyre T., Muelbert M., Patterson T., Roquet F., Williams G. & Charrassin J.B. 2016. Circumpolar habitat use in the southern elephant seal: implications for foraging success and population trajectories. Ecosphere 7, e01213, doi: 10.1002/ecs2.1213.

Hofmeyr G.J.G., Krafft B.A., Kirkman S.P., Bester M.N., Lydersen C. & Kovacs K.M. 2005. Population changes of Antarctic fur seals at Nyrøysa, Bouvetøya. Polar Biology 28, 725–731, doi: 10.1007/s00300-005-0732-7.

Huyser O. 2001. Bouvetøya (Bouvet Island). In M.I. Evans & L.D.C. Fishpool (eds.): Important bird areas in Africa and associated islands: priority sites for conservation. Pp. 113–115. Newbury, UK: Pisces Publications and BirdLife International.

Inoshima Y., Morooka A. & Sentsui H. 2000. Detection and diagnosis of parapoxvirus by the polymerase chain reaction. Journal of Virological Methods 84, 201–208, doi: 10.1016/S0166-0934(99)00144-5.

Jensen S.K., Aars J., Lydersen C., Kovacs K.M. & Åsbakk K. 2010. The prevalence of Toxoplasma gondii in polar bears and their marine mammal prey: evidence for a marine transmission pathway? Polar Biology 33, 599–606, doi: 10.1007/s00300-009-0735-x.

Jensen S.K., Nymo I.H., Forcada J., Godfroid J. & Hall A. 2012. Prevalence of Toxoplasma gondii antibodies in pinnipeds from Antarctica. Veterinary Records 171, 249–249, doi: 10.1136/vr.100848.

Jensen S.K., Nymo I.H., Forcada J., Hall A. & Godfroid J. 2013. Brucella antibody seroprevalence in Antarctic seals (Arctocephalus gazella, Leptonychotes weddellii and Mirounga leonina). Disease of Aquatic Organisms 105, 175–181, doi: 10.3354/dao02633.

Kirkman S.P., Hofmeyr G.J.G., Bester M.N. & Isaksen K. 2001. Counts of southern elephant seals, Mirounga leonina, at Bouvet Island. Polar Biology 24, 62–65, doi: 10.1007/s003000000180.

Klein J. & Tryland M. 2005. Characterisation of parapoxviruses isolated from Norwegian semi-domesticated reindeer (Rangifer tarandus tarandus). Virology Journal 2, article no. 79, doi: 10.1186/1743-422X-2-79.

Kumar S., Stecher G., Li M., Knyaz C. & Tamura K. 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549, doi: 10.1093/molbev/msy096.

Larsen A.K., Nymo I.H., Boysen P., Tryland M. & Godfroid J. 2013. Entry and elimination of marine mammal Brucella spp. by hooded seal (Cystophora cristata) alveolar macrophages in vitro. PLoS One 8, e70186, doi: 10.1371/journal.pone.0070186.

Lindsay D.S. & Dubey J.P. 2009. Long-term survival of Toxoplasma gondii sporulated oocysts in seawater. Journal of Parasitology 95, 1019–1021, doi: 10.1645/GE-1919.1.

Lloyd-Smith J.O., Greig D.J., Hietala S., Ghneim G.S., Palmer L., St Leger J., Grenfell B.T. & Gulland F.M. 2007. Cyclical changes in seroprevalence of leptospirosis in California sea lions: endemic and epidemic disease in one host species? BMC Infectious Diseases 7, article no. 125, doi: 10.1186/1471-2334-7-125.

Mazzariol S., Marcer F., Mignone W., Serracca L., Goria M., Marsili L., Di Guardo G. & Casalone C. 2012. Dolphin morbillivirus and Toxoplasma gondii coinfection in a Mediterranean fin whale (Balaenoptera physalus). BMC Veterinary Research 8, article no. 20, doi: 10.1186/1746-6148-8-20.

McDonald W.L., Jamaludin R., Mackereth G., Hansen M., Humphrey S., Short P., Taylor T., Swingler J., Dawson C.E., Whatmore A.M., Stubberfield E., Perrett L.L. & Simmons G. 2006. Characterization of a Brucella sp. strain as a marine-mammal type despite isolation from a patient with spinal osteomyelitis in New Zealand. Journal of Clinical Microbiology 44, 4363–4370, doi: 10.1128/JCM.00680-06.

McFarlane R.A. 2009. Health assessment and diseases of the Weddell seal, Leptonochotes weddelli, in Vestfold Hills, East Antarctica. In K.R. Kerry & M.J. Riddle (eds.): Health of Antarctic wildlife. Pp. 139–166. Berlin: Springer.

Miller M.A., Gardner I.A., Kreuder C., Paradies D.M., Worcester K.R., Jessup D.A., Dodd E., Harris M.D., Ames J.A., Packham A.E. & Conrad P.A. 2002. Coastal freshwater runoff is a risk factor for Toxoplasma gondii infection of southern sea otters (Enhydra lutris nereis). International Journal of Parasitology 32, 997–1006, doi: 10.1016/S0020-7519(02)00069-3.

Müller G., Gröters S., Siebert U., Rosenberger T., Driver J., König M., Becher P., Hetzel U. & Baumgärtner W. 2003. Parapoxvirus infection in harbor seals (Phoca vitulina) from the German North Sea. Veterinary Pathology 40, 445–454, doi: 10.1354/vp.40-4-445.

Nollens H.H., Gulland F.M., Hernández J.A., Condit R.C., Klein P.A., Walsh M.T. & Jacobson E.R. 2006. Seroepidemiology of parapoxvirus infections in captive and free-ranging California sea lions Zalophus californianus. Diseases of Aquatic Organisms 69, 153–161, doi: 10.3354/dao069153.

Nollens H.H., Gulland F.M., Jacobson E.R., Hernández J.A., Klein P.A., Walsh M.T. & Condit R.C. 2006. Parapoxviruses of seals and sea lions make up a distinct subclade within the genus Parapoxvirus. Virology 349, 316–324, doi: 10.1016/j.virol.2006.01.020.

Nymo I.H., Arias M.A., Pardo J., Álvarez M.P., Alcaraz A., Godfroid J. & de Bagüés M.P.J. 2016. Marine mammal Brucella reference strains are attenuated in a BALB/c mouse model. PLoS One 11, e0150432, doi: 10.1371/journal.pone.0150432.

Nymo I.H., Godfroid J., Åsbakk K., Larsen A.K., das Neves C.G., Rødven R. & Tryland M. 2013. A protein A/G indirect enzyme-linked immunosorbent assay for the detection of anti-Brucella antibodies in Arctic wildlife. Journal of Veterinary Diagnostics Investigations 25, 369–375, doi: 10.1177/1040638713485073.

Osterhaus A.D., Broeders H.W., Visser I.K., Teppema J.S. & Kuiken T. 1994. Isolation of a parapoxvirus from pox-like lesions in grey seals. Veterinary Records 135, 601–602, doi: 10.1136/vr.135.25.601.

Osterhaus A.D.M.E., Yang H., Spijkers H.E.M., Groen J., Teppema J.S. & Van Steenis G. 1985. The isolation and partial characterization of a highly pathogenic herpesvirus from the harbor seal (Phoca vitulina). Archives of Virology 86, 239–251, doi: 10.1007/BF01309828.

Palmgren H., McCafferty D., Aspan A., Broman T., Sellin M., Wollin R., Bergström S. & Olsen B. 2000. Salmonella in sub-Antarctica: low heterogeneity in Salmonella serotypes in South Georgian seals and birds. Epidemiology & Infection 125, 257–262, doi: 10.1017/S0950268899004586.

Rengifo-Herrera C., Ortega-Mora L.M., Álvarez-García G., Gómez-Bautista M., García-Párraga D., García-Peña F.J. & Pedraza-Díaz S. 2012. Detection of Toxoplasma gondii antibodies in Antarctic pinnipeds. Veterinary Parasitology 190, 259–262, doi: 10.1016/j.vetpar.2012.05.020.

Retamal P., Blank O., Abalos P. & Torres D. 2000. Detection of anti-Brucella antibodies in pinnipeds from the Antarctic territory. Veterinary Records 146, 166–167, doi: 10.1136/vr.146.6.166.

Ross P.S. 2002. The role of immunotoxic environmental contaminants in facilitating the emergence of infectious diseases in marine mammals. Human and Ecological Risk Assessments 8, 277–292, doi: 10.1080/20028091056917.

Scotter S.E., Tryland M., Nymo I.H., Hanssen L., Harju M., Lydersen C., Kovacs K.M., Klein J., Fisk A.T. & Routti H. 2019. Contaminants in Atlantic walruses in Svalbard part 1: relationships between exposure, diet and pathogen prevalence. Environmental Pollution 244, 9–18, doi: 10.1016/j.envpol.2018.10.001.

Sidor I., Goldstein T., Whatmore A.M., Zabka T.S., Frasca S., Gulland F.M.D. & Dunn J.L. 2008. Transplacental infection with Brucella in California sea lion (Zalophus californianus) fetus. Paper presented at Brucellosis 2008 International Research Conference, 10–13 September, London.

Smeele Z.E., Burns J.M., Van Doorsaler K., Fontenele R.S., Waits K., Stainton D., Shero M.R., Beltran R.S., Kirkham A.L., Berngartt R., Kraberger S. & Varsani A. 2018. Diverse papillomaviruses identified in Weddell seals. The Journal of General Virology 99, 549–557, doi: 10.1099/jgv.0.001028.

Sohn A.H., Probert W.S., Glaser C.A., Gupta N., Bollen A.W., Wong J.D., Grace E.M. & McDonald W.C. 2003. Human neurobrucellosis with intracerebral granuloma caused by a marine mammal Brucella spp. Emerging Infectious Diseases 9, 485–488, doi: 10.3201/eid0904.020576.

Stenvers O., Plötz J. & Ludwig H. 1992. Antarctic seals carry antibodies against seal herpesvirus. Archives of Virology 123, 421–424, doi: 10.1007/BF01317275.

Tamura K. 1992. Estimation of the number of nucleotide substitutions when there are strong transition--transversion and G+ C-content biases. Molecular Biology and Evolution 9, 678–687, doi: 10.1093/oxfordjournals.molbev.a040752.

Tischer B.K. & Osterrieder N. 2010. Herpesviruses—a zoonotic threat? Veterinary Microbiology 140, 266–270, doi: 10.1016/j.vetmic.2009.06.020.

Tryland M. 2011. Seal parapoxvirus. In D. Liu (ed.): Molecular detection of human viral pathogens. Pp. 1029–1037. Boca Raton: CRC Press.

Tryland M. 2017. Zoonoses and public health. In F.M.D. Gulland et al. (eds.): CRC handbook of marine mammal diseases. 2nd edn. Pp. 47–62. Boca Raton: CRC Press.

Tryland M., Klein J., Nordøy E.S. & Blix AS. 2005. Isolation and partial characterization of a parapoxvirus isolated from a skin lesion of a Weddell seal. Virus Research 108, 83–87, doi: 10.1016/j.virusres.2004.08.005.

Tryland M., Nymo I.H., Nielsen O., Nordøy E.S., Kovacs K.M., Krafft B.A., Thoresen S.I., Åsbakk K., Osterrieder K., Roth S.J., Lydersen C., Godfroid J. & Blix A.S. 2012. Serum chemistry and antibodies against pathogens in Antarctic fur seals, Weddell seals, crabeater seals, and Ross seals. Journal of Wildlife Diseases 48, 632–645, doi: 10.7589/0090-3558-48.3.632.

Varsani A., Frankfurter G., Stainton D., Male M.F., Kraberger S. & Burns J.M. 2017. Identification of a polyomavirus in Weddell seal (Leptonychotes weddellii) from the Ross Sea (Antarctica). Archives of Virology 162, 1403–1407, doi: 10.1007/s00705-017-3239-y.

Whatmore A.M., Dawson C.E., Groussaud P., Koylass M.S., King A.C., Shankster S.J., Sohn A.H., Probert W.S. & McDonald, W.L. 2008. Marine mammal Brucella genotype associated with zoonotic infection. Emerging Infectious Diseases 14, 517–518, doi: 10.3201/eid1403.070829.

Whatmore A.M., Dawson C., Muchowski J., Perrett L.L., Stubberfield E., Koylass M., Foster G., Davis N.J., Quance C., Sidor I.F., Field C.L. & St Leger J. 2017. Characterisation of North American Brucella isolates from marine mammals. PloS One 12, e0184758, doi: 10.1371/journal.pone.0184758.
How to Cite
Núñez-Egido, S., Lowther, A., Nymo, I. H., Klein, J., Breines, E. M., & Tryland, M. (2020). Pathogen surveillance in Southern Ocean pinnipeds. Polar Research, 39.
Research Articles