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Influenza detected in Macronectes giganteus in two islands of South Shetlands, Antarctica

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Influenza A virus was detected in different species of birds and migratory aquatic birds. They are the main reservoir of the virus. In this research we detected the first Influenza A virus in Southern Giant Petrel in an Antarctic region. The results represent 0.33% of the samples collected in two breeding areas of the species. Some factors can explain the introduction of these pathogens and diseases in Antarctica, such as bird’s migratory behavior and the remains of the virus in cold waters.
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Science Highlights - Thematic Area 2 |
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INFLUENZA DETECTED IN Macronectes giganteus
IN TWO ISLANDS OF SOUTH SHETLANDS, ANTARCTICA
Elisa de Souza Petersen1*, Maria Virginia Petry1, Édison Durigon2, Jansen Araújo2
1Universidade do Vale do Rio dos Sinos – UNISINOS, Laboratório de Ornitologia e Animais Marinhos,
Av
.
Unisinos, nº 950, Cristo Rei, 93.022-000, São Leopoldo, Rio Grande do Sul, Brazil
2Universidade de São Paulo – USP, Laboratório de Virologia Clínica e Molecular,
Av. Prof. Lineu Prestes, 1374, 05508-900, 2º andar, São Paulo, Brazil
*email: elisapetersen@yahoo.com.br
Abstract: Inuenza A virus was detected in dierent species of birds and migratory aquatic birds. ey are the main reservoir
of the virus. In this research we detected the rst Inuenza A virus in Southern Giant Petrel in an Antarctic region. e results
represent 0.33% of the samples collected in two breeding areas of the species. Some factors can explain the introduction of these
pathogens and diseases in Antarctica, such as bird’s migratory behavior and the remains of the virus in cold waters.
Keywords: Southern Giant Petrel, Viruses, Elephant Island, King George Island
Introduction
Influenza A has been detected in humans, pigs,
horses, marine mammals and in dierent species of birds
(Websteretal., 1992). Currently 105 species of wild birds
have been detected with Inuenza A and aquatic birds are
the main reservoir of the virus (Olsenet al., 2006). e
transmission is poorly understood (Alexander, 2007),
however the easiest form of spreading of the virus is in water,
remaining infective for 30 days in 0°C (Webster etal., 1978).
In Antarctica Sphenisciformes, Procellariiformes and
Charadriiformes breed during the austral summer. Most
are long-distance migratory species, excluding penguins,
and are observed in diverse and dense colonies in ice free
areas (Schreiber & Burger, 2002). However, these breeding
areas are scarse hence the proximity of the colonies and
the nests make the intra and interespecic transmission
of the virus easier. The Southern Giant Petrel (SGP)
(Macronectes giganteus) breeds in the Antarctic region and
has a circumpolar distribution (Pattersonetal., 2008) and
with other species of seabirds became a potential disperser
of several diseases. Barbosa & Palacius (2009) presented a
review of main parasites and diseases detected in Antarctic
seabirds and associated dierent microorganism to SGP.
erefore, the migratory behavior and the presence of
several diseases make the SGP an important species to
research, not only for the species conservation but for
the Antarctic ecosystem. e objective of this research is
detecting the Inuenza A virus in SGP in two regions in
South Shetland Island.
Materials and Methods
The data was collected at Stinker Point (Elephant
Island) and Admiralty Bay (King George Island), South
Shetlands Island, during three breeding seasons. Two
tracheal and cloacal samples were collected from adults
and chicks (Figure 1), all the animals were banded to avoid
the recapture. e detection was conducted in Biossecurity
level 3+ Laboratory. To RNA extraction we used NucliSENS®
easyMAG® (Biomérieux) Kit. e viral detection was made
by RT-PCR with TaqMan® Avian Inuenza Virus (AIV-M)
Reagents.
DOI: http://dx.doi.org/10.4322/apa.2015.004
36 | Annual Activity Report 2013
reported with some virus infection. Barbosa & Palacius
(2009) presented a review about the health of Antarctic
and sub-Antarctic seabirds describing nine species with
six dierent virus infection. ese species are six penguins
(Aptenodytes patagonicus, A. forsteri, Pygoscelis papua, P.
adeliae, P. antarctica, Eudyptes chrysolophus, E. schlegeli),
one petrel (Macronectes giganteus) and one species of
skua (Stercorarius maccormicki). However the research
results show the presence of viral antibody instead of the
virus. In South Shetland Island, the same study area of this
research, antibody of H1, H3, H7 H9 of Inuenza were
detected in adults and chicks of P. antarctica, P. adeliae,
Results
A major number of tracheal and cloacal samples were
collected in Elephant Island (Table 1). Inuenza A virus
was detected in one individual, representing 0,33% of all
individuals manipulated. All the samples of Admiralty Bay
were negative to virus Inuenza A. e detection occurred
in a male in Elephant Island (Figure 2). is individual was
captured during the 2010/11 austral Summer, January 9th.
Discussion
Despite the SGP that was detected with Inuenza A virus
in Antarctica, dierent Antarctic seabirds species have been
Table 1. Samples collected during the three breeding seasons of Southern Giant Petrel in Elephant Island (EI) and King George Island (KG).
2009/10 2010/11 2011/12 Total
EI KG EI KG EI KG
Males 36 7 30 4 77
Female 39 10 31 11 91
Chicks 15 58 8 50 131
Total 15 0 133 25 111 15 299
Figure 1. A. Southern Giant Petrel chick in Elephant Island.
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Science Highlights - Thematic Area 2 |
P.papua, Stercorarius sp and M. giganteus. e data of this
research is similar to preview information, showing that
most individuals in the area are not infected. Nevertheless,
one individual representing 0.33% of the total sample was
detected with Inuenza A, emphasizing the importance of
the research about Antarctic health.
Regardless of the Antarctic being considered as an
isolated environment, this area is impacted by other
environments in the planet, as well as by other organisms,
like pathogens and diseases. Some factors can explain
the introduction of these pathogens and diseases in
Antarctica: bird’s migratory behavior (Kraussetal., 2007;
Olsenetal., 2006) and the remains of the virus in cold waters
(Zhangetal., 2006).
Conclusion
rough this data it was possible to detect Inuenza A
virus in SGP in the Antarctic region. Despite the low number
of individuals contaminated, with only one positive result
for the virus among two study areas, it is suggested that
new research should be performed. is new data would
involve migratory and resident species of dierent areas in
Antarctica, like the Peninsula, the Continent and boundary
islands. e transmission of the virus may be facilitated
because of the proximity of the nests of the species during
their breeding seasons and by the sharing of cold water areas,
thus, lake sediments and water could also be analyzed. ese
breeding groups should be kept under monitoring to verify
the permanence of virus in these seabirds.
Acknowledgements
is work integrates the National Institute of Science
and Technology Antarctic Environmental Research (INCT-
APA) that receives scientic and nancial support from the
National Council for Research and Development (CNPq
process: n° 574018/2008-5) and Carlos Chagas Research
Support Foundation of the State of Rio de Janeiro (FAPERJ
n° E-16/170.023/2008). e authors also acknowledge the
support of the Brazilian Ministries of Science, Technology
and Innovation (MCTI), of Environment (MMA) and Inter-
Ministry Commission for Sea Resources (CIRM).
Figure 2. Southern Giant Petrel adults in Elephant Islands.
38 | Annual Activity Report 2013
References
Alexander, D. J. (2007). An overview of the epidemiology of avian influenza. Vaccine, 25, 5637-5644. PMid:17126960. http://
dx.doi.org/10.1016/j.vaccine.2006.10.051
Barbosa, A., & Palacios, M. J. (2009). Health of Antarctic birds: a review of their parasites, pathogens and disease. Polar
Biology, 32, 1095-1015. http://dx.doi.org/10.1007/s00300-009-0640-3
Krauss, S., Obert, C. A., Franks, J., Walker, D., Jones, K., Seiler, P. et al. (2007). Influenza im migratory birds and evidence
of limited intercontinental virus exchange. Plos Pathogens, 3, 1684-1693. PMid:17997603 PMCid:PMC2065878. http://
dx.doi.org/10.1371/journal.ppat.0030167
Olsen, B., Munster, V. J., Wallensten, A., Waldenstrom, J., Osterhaus, A. D. M. E., & Fouchier, R. A. (2006). Global patterns
of Influenza A virus wild birds. Science, 312, 384-388. PMid:16627734. http://dx.doi.org/10.1126/science.1122438
Patterson, D. L., Woehler, E. J., Croxall, J. P., Cooper, J., Poncet, S., Peter, H. U. et al. (2008). Breeding distribution and
population status of the northern giant petrel Macronectes halli and the southern giant petrel M. giganteus. Marine Ornithology,
36, 115-124.
Schreiber, E. A., & Burger. J. (2002). Biology of marine birds. Boca Raton: CRC Press. 219 p.
Webster, R. G., Yaknot, M., Hinshaw, V. S., Bean, W. J., & Murti, K. C. (1978). Intestinal Influenza: replication and characterization
of influenza virus in ducks. Virology, 84, 268-278. http://dx.doi.org/10.1016/0042-6822(78)90247-7
Webster, R. G., Bean, W. J., Gorman, O. T., Chambers, T. M., & Kawaoka, Y. (1992). Evolution and Ecology of Influenza A
viruses. Microbiological Reviews, 56, 152-179. PMid:1579108 PMCid:PMC372859
Zhang, G., Shoham, D., Gilichinsky, D., Davydov, S., Castello, J. D., & Rogers, S. O. (2006). Evidence of Influenza A virus RNA
in Siberian Lake Ice. Journal of Virology, 80, 12229-12235. PMid:17035314 PMCid:PMC1676296. http://dx.doi.org/10.1128/
JVI.00986-06
... There are three reports on pathogen shedding diagnosed by PCR. Two are based on swabs from apparently healthy chicks including Amsterdam Albatross (sample size unknown) for P. multocida and E. rhusiopathiae , and one Southern Giant Petrel for Influenza A virus (de Souza Petersen et al. 2015 ). The potential significance of the finding in apparently healthy Amsterdam Albatross chicks has been discussed above, yet without further details, it remains speculative at best. ...
... I. uriae ticks (3/41) from Black-browed Albatross breeding in Campbell Island, New Zealand, were positive for the vectorborne bacteria Borrelia garinii DNA by PCR(Olsen et al. 1995 ). Recently (2010/11 austral summer), Influenza A virus RNA was detected by Reverse Transcription PCR (RT-PCR) in swabs from one (1/299) male Southern Giant Petrel of undescribed age from Elephant Island, Antarctica(de Souza Petersen et al. 2015 ). It is unknown whether the isolate was from a cloacal or oral swab. ...
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Intestinal Influenza: replication and characterization of influenza virus in ducks
  • R G Webster
  • M Yaknot
  • V S Hinshaw
  • W J Bean
  • K C Murti
Webster, R. G., Yaknot, M., Hinshaw, V. S., Bean, W. J., & Murti, K. C. (1978). Intestinal Influenza: replication and characterization of influenza virus in ducks. Virology, 84, 268-278. http://dx.doi.org/10.1016/0042-6822(78)90247-7