New Results

Detection and spread of high pathogenicity avian influenza virus H5N1 in the Antarctic Region

Ashley Bennison, Alexander M. P. Byrne, Scott M. Reid, Joshua G. Lynton-Jenkins, Benjamin Mollett, Dilhani De Sliva, Jacob Peers-Dent, Kim Finlayson, Rosamund Hall, Freya Blockley, Marcia Blyth, Marco Falchieri, Zoe Fowler, Elaine M. Fitzcharles, Ian H. Brown, Joe James, Ashley C. Banyard
doi: https://doi.org/10.1101/2023.11.23.568045

Abstract

The Antarctic is the only major geographical region in which high pathogenicity avian influenza virus (HPAIV) has never previously been detected. The current panzootic of H5N1 HPAIV has decimated wild bird populations across Europe, North America and South America. Here we report on the emergence of clade 2.3.4.4b H5N1 HPAIV in the Antarctic and sub-Antarctic regions of South Georgia and the Falkland Islands respectively. We initially detected H5N1 HPAIV in samples collected from brown skuas at Bird Island, South Georgia on 8th October 2023. Since this detection, increased mortalities were observed in brown skuas, kelp gulls, elephant seals and fur seal at multiple sites across South Georgia. We confirmed H5N1 HPAIV in multiple brown skuas and kelp gulls across four different sampling locations in South Georgia. Simultaneously, we also confirmed H5N1 HPAIV in a southern fulmar in the Falkland Islands. Genetic assessment of the virus indicates spread from South America, likely through movement of migratory birds. Here we describe the emergence, species impact and genetic composition of the virus and propose both introductory routes and potential long-term impact on avian and mammalian species across the Antarctic region.

Introduction

Following the emergence and global expansion of A/goose/Guangdong/1/96 (GsGd)-lineage H5 high pathogenicity avian influenza viruses (HPAIV) there have been repeat epizootics in wild birds and poultry populations globally. In the autumn of 2021, the situation escalated considerably with the detection of clade 2.3.4.4b HPAIV subtype H5N1 in Europe. Subsequently, two unprecedented epizootic waves in 2021/22 and 2022/23 with this lineage were associated with mass mortality events in wild birds together with thousands of incursions into poultry1, 2, 3, 4, 5. High levels of viral adaptation to wild bird species6, and increased fitness advantage through continued genetic reassortment7 likely underpin the broad impact infection has had across many avian species2. This wide host range has facilitated the transmission of the lineage across a large geographic area, including from Europe to North America8, 9, where it has since rapidly expanded its range southward into South America via migratory avian species. Incursion into South American countries, starting in November of 2022, represented the first recorded instances of GsGd-lineage H5 HPAIV in the region10, 11, 12. Mass mortality events in the region have been particularly severe and reported across several different bird species in addition to marine mammals2, 10, 13, highlighting the extensive ecological impact of HPAIV and the ongoing threat it presents to naïve hosts.

The Antarctic region includes the ice shelves, waters, and all the island territories in the Southern Ocean situated inside of the Antarctic Convergence, a marine belt encircling Antarctica where Antarctic waters meet those of the warmer sub-Antarctic. Several islands are located inside the Antarctic region, including South Georgia, while the Falkland Islands among others are located outside the Antarctic Convergence in the sub-Antarctic zone. There have been no previous reports of HPAIV inside the Antarctic region14. Antarctica and the sub-Antarctic islands possess unique ecosystems which support the population strongholds of several avian and marine mammal species. The relative isolation of these islands from human populations has provided species across the Antarctic with only limited protection from anthropogenic environmental change15. Indeed, wildlife populations in the Antarctic face a broad range of challenges from introduced species16, to longline fisheries17, 18, and rapid climate change19, 20, 21. Several resident bird species including wandering albatross (Diomedea exulans), macaroni penguins (Eudyptes chrysolophus), grey-headed albatross (Thalassarche chrysostoma), and white-chinned petrel (Procellaria aequinoctialis), are listed as either vulnerable or endangered22. Iconic long-lived species with late maturity, such as albatross, exhibit low resilience to rapid increases in population mortality23. High mortality disease outbreaks therefore represent a substantial threat to already vulnerable seabird populations24, 25.

While geographically isolated, several Antarctic seabird species routinely range between the South Atlantic and Southern Ocean, visiting the South American coast to either forage or overwinter26. Brown skuas (Stercorarius antarcticus), kelp gulls (Larus dominicanus), southern giant petrel (Macronectes giganteus), and snowy sheathbills (Chionis albus) have previously been identified as potential vectors of infectious pathogens into this vulnerable ecosystem due to their migratory traits, scavenging behaviour, and previously identified roles as carriers of low pathogenicity avian influenza viruses (LPAIV)27, 28, 29, 30, 31, 32, 33, 34. Evidence of low pathogenicity avian influenza virus (LPAIV) in the Antarctic region was first detected from serological studies in the 1980s35, 36, 37. A range of subtypes have since been reported (H137, H328, H432, H538, H629, H736, H928, and H1130) including genetic analysis of H4N732, H5N530, 38, H6N829 and H11N230, 39, 40 influenza viruses. In contrast to the more prevalent H11N2 viruses, H4-H6 subtypes were found to share high sequence similarity with viruses from continental America, indicating more recent introduction events29, 30, 32.

Evidence of likely LPAIV transmission to the continent from the Americas demonstrates the high-risk of clade 2.3.4.4b H5 HPAIV introduction to the Antarctic, encouraging researchers in 2022 to employ additional biosecurity measures while maintaining surveillance activities27, 41. During the austral summer of 2022/23, sampling and surveillance was conducted at several sites in the Antarctic region, and as of March 2023, HPAIV had not been detected14.

Here we describe the observation of morbidity and mortality events across different species as well as the positive detection of H5N1 HPAIV in a variety of species in South Georgia, inside the Antarctic region and the sub-Antarctic Falkland Islands. We detail the suspicion, emergence, diagnostic evaluation and clinical presentations of HPAIV in the region. Genetic analysis is used to characterise potential introduction routes and the consequences of HPAIV circulation in this region are considered.

Results

Case description

On September 17th, researchers of the British Antarctic Survey (BAS) on Bird Island, South Georgia, (Figure 1A) discovered a single southern giant petrel showing behaviours indicative of loss of coordination, neurological twitching, and lethargy. This individual was observed being predated and scavenged upon by brown skuas and other southern giant petrels. On 8th October, brown skuas were observed in the same locality showing lethargy, neck spasms, twitching, and an inability to fly, and by 10th October, these individuals had died (Figure 1B). In the following days bird mortality was seen on Bird Island, South Georgia, with the highest number of mortalities occurring at the roosting site of non-breeding birds. Swab samples were collected from the three brown skua (Stercorarius antarcticus) on 8th October 2023 which were later found dead on Bird Island, South Georgia (Figure 1B). Mortalities increased rapidly in brown skuas, with ten birds recorded dead by 15th October 2023 and a further twenty birds by 20th October. Further escalation in mortality occurred by 17th November 2023, when 57 skuas were observed to have died at Bird Island, and close monitoring continues.

Figure 1.
Figure 1. Geographical distribution of H5N1 HPAIV detections from South Georgia.

(A) Map showing the locations of South America (blue), the Falkland Islands (red), South Georgia (green) and the Antarctic peninsula (yellow). (B) Map showing the location, species, and date of sampling of avian and mammalian species in South Georgia.

On 30th October, swab samples were collected from six found dead kelp gull and four found dead brown skua from Hound Bay, South Georgia in addition to four found dead brown skua from St Andrews, South Georgia (Figure 1B). On 31st of October, swab samples were collected from six kelp gulls, and six brown skuas which were found dead in Moltke Harbour, South Georgia. On 3rd November, samples were collected from six found dead kelp gulls and two brown skuas on Harpon, South Georgia (Figure 1B). Alongside avian species, clinical disease consistent with mammalian infection with HPAIV was observed in colonies of elephant seals. Clinical presentation included difficulty breathing, with coughing and short sharp breath intake. Individuals also showed accumulation of viscous fluid around the nasal passage. Swab samples were collected from seven recently deceased southern elephant seals (Mirounga leonine) on 31st October from Moltke Harbour, South Georgia (Figure 1B).

Concurrent to the events emerging on South Georgia, on 30th October, a southern fulmar (Fulmarus glacialoides) was reported dead in Stanley, Falkland Islands and swab samples were collected (Figure 1A). Over the next few days mortality was seen in other avian species in Stanley, and samples were collected from a Grey-backed storm petrel (Garrodia nereis) and Falkland steamer duck (Tachyeres brachypterus) on 6th November.

Virology and detection

Provision for diagnostic investigation of avian influenza is limited in the region. Local molecular testing at the KEMH Pathology and Food, Water & Environmental Laboratory on the Falkland Islands indicated the presence of avian influenza A H5N1 viral RNA (vRNA) in a Southern Fulmar. This detection, alongside the increase clinical disease and mortalities observed on South Georgia triggered shipment of samples to the International Reference Laboratory for avian influenza, swine influenza and Newcastle disease virus at the Animal and Plant Health Agency (APHA), Weybridge, UK for confirmatory and further diagnostic evaluation. All six oropharyngeal (OP) and cloacal (C) swabs from the three brown skuas from South Georgia collected on 8th October were positive by each of the generic AIV, HPAIV H5 detection and N1-specific rRT-PCR assays (Supplementary Table 1), signifying the presence of HPAIV H5N1 in all three birds. However, infectious virus could not be isolated from any of these samples. Eighteen additional OP and C swab samples from brown skuas (n=12) and kelp gulls (n=6) sampled from four sites across South Georgia between 30th October and 3rd of November also all tested positive for the presence of H5N1 HPAIV vRNA (Supplementary Table 1). Infectious virus was successfully isolated from four birds, including from one kelp gull and two brown skuas from Hound Bay and one kelp gull at Harpon Bay. Nasal and rectal swabs from three elephant seals collected on Moltke Harbour on 3rd November were negative in each assay, and no infectious virus could be isolated from these animals. Within the same period samples collected from a southern fulmar on 30th October in the Falkland Islands tested positive for HPAIV H5N1 vRNA, while a Grey-backed storm petrel and Falkland steamer duck tested negative in each assay.

Genomic and phylogenetic analysis

Three full genome sequences were generated from the initial OP swab samples of the three brown skuas from Bird Island collected on 8th October 2023. Comparison of the three sequences revealed that they shared 99.86-100% nucleotide identity across all eight influenza viral gene segments. In addition, a single sequence was also generated from the Southern Fulmar collected from the Falkland Islands on 30th October 2023. Comparison of the sequences obtained from South Georgia and the Falkland Islands found that they shared greater than 98.98% nucleotide identity across all gene segments. The Bird Island and Falkland Islands sequences were then combined with representative global H5N1 clade 2.3.4.4b full-genome sequences to assess genetic ancestry (Supplementary Figure 1). The sequences from Bird Island clustered with those of viruses collected from South America, between December 2022 and April 2023, particularly Uruguay, Peru and Chile, across all gene segments. The sequences from Bird Island and the Falkland Islands were genotyped according to the United States H5N1 schema, given the spread of these viruses from North to South America in early 202210, and found to be part of the B3.2 genotype42. The B3.2 genotype arose in early 2022 in North Dakota as a reassortant formed by the original H5N1 that was transmitted from Europe to North America in late 20218 and then obtained gene segments (PB2, PB1, NP and NS) from local North American AIVs42. This genotype was reported to have been introduced into South America four times between October 2022 and March 202310, and analysis of all publicly available full-genome sequences from South America found that 94% (131 of 140) of H5N1 belonged to this genotype.

To further investigate the introduction of H5N1 HPAIV into South Georgia and the Falkland Islands, representative H5N1 clade 2.3.4.4b HA sequences from North and South America were used to perform time-resolved phylogenetic analysis (Figure 2). This analysis demonstrated distinct, separate introductions of H5N1 into South Georgia and the Falkland Islands, with both sets of sequences sharing a common ancestor with sequences from South America dating between late November 2022 (Falkland Islands) and late January 2023 (South Georgia). However, both sets of sequences produced long branch lengths compared to South American sequences. To further investigate the source of these viruses, discrete trait analysis based upon the country of origin was performed (Supplementary Figure 2), which suggested that the source of HPAIV for both South Georgia and the Falkland Islands was Chile.

Figure 2.
Figure 2. H5N1 HPAIV transmission from the South American continent to Falkland Islands and South Georgia.

(A) Representative haemagglutinin (HA) sequences H5N1 HPAIVs from North and South America were combined with those obtained from South Georgia and the Falkland Islands and used to generate a time-resolved maximum-likelihood phylogenetic tree and coloured according to origin location.

Discussion

Since the emergence and global expansion of Gs/Gd-lineage H5Nx HPAIV in 1996, Antarctica and Oceania are the only two continents in which it has not been detected. Moreover, until now, Antarctica remains the only major geographical region in which HPAIV had never been detected.

The island of South Georgia lies in the Southern Ocean inside the Antarctic convergence, a marine belt encircling Antarctica which defines the Antarctic Region. The island is an area of high biodiversity and high conservation priority with multiple species being considered as vulnerable to the incursion of infectious diseases43, 44, 45. The Falkland Islands constitute a remote cluster of islands in the South Atlantic Ocean situated approximately 1500km to the west of South Georgia. The Falkland Islands are situated outside of the Antarctic convergence, in the sub-Antarctic region. Both the Falkland Islands archipelago and South Georgia represent key areas that are host to significant avian biodiversity and the presence of HPAIV on these islands represents a significant risk to the populations of susceptible bird species. South Georgia is home to approximately 29 species which breed on the islands and is recognised as an ‘Important Bird Area’ by Birdlife International46.

Therefore, any colony or population that comes under threat from an HPAIV outbreak on South Georgia may have direct impact upon the wider population of seabirds. Despite seabird colonies showing space partitioning between colonies47, there is often a high degree of connectivity between colonies. Often this is due to the movement of nonbreeders or juvenile birds48. It is therefore, not unreasonable to suspect that birds on South Georgia may show high connectivity, which may aid the spread of disease, as has been documented previously33, but also may be evidenced by the rapid collection of samples from different areas within South Georgia. Indeed, in the northern hemisphere it has been found that northern gannets (Morus bassanus) increased their connectivity due to high levels of colony prospecting from surviving birds49.

This connectivity and the interlinkages between avian and mammalian species in a ‘single ecosystem’ having been identified across the Antarctic region means that the virus may be readily spread across the region. Circumpolar and trans-Pacific migrants such as Gray-headed albatross (Thalassarche chrysostoma)50, White-chinned petrel (Procellaria aequincotialis)51, Northern and southern giant petrels may facilitate this spread. Indeed, phylogeographic analysis has suggested a dynamic geneflow between southern Atlantic populations and Macquarie island52, and as such the threat of transmission to New Zealand and Australasia must be considered.

From a mammalian infection standpoint there have been several reports globally of wild aquatic mammals, including seals, being infected with H5Nx HPAIV since 2020, where infection has been attributed to the predation of sick or dead infected birds10, 53, 54. Information to date suggests that HPAIV infection in seals often leads to a neurological presentation with infrequent detection of viral material being detected through standard swab sampling activities53. This may explain the lack of influenza A vRNA detection in elephant seal swab samples taken from this study, despite the consistency of clinical presentation seen in elephant seals with that reported elsewhere. Certainly, the timing of mortality and clinical signs exhibited by elephant seals are consistent with HPAIV infection. Unfortunately, invasive sampling was prohibited in this study due to a lack of personal and respiratory protective equipment to safely undertake such sampling and invasive sampling of avian and mammalian species remains challenging to undertake in areas where appropriate facilities are lacking.

A further conundrum that will likely significantly impact upon the course of infection and onward spread of viral infection across the region is the limited options for carcass disposal and environmental clean-up. The Antarctic region is one of the most remote environments on earth and is the location of enormous breeding colonies of various avian species that may be susceptible, and succumb, to infection with HPAIV. Where mortality events occur, the opportunity for scavenging animals exists to predate upon carcasses and become infected. Carcass removal is not an option.

Further the potential for virus survival in this cold environment is increased and it may be that infectious virus remains for longer periods in carcasses preserved by the local climate. Local ecology of species could also influence the scale of impact throughout Antarctica. Although all species remain vulnerable to large scale infection events, it is possible that the density of animals may preclude some species from rapid spread55. For example, wandering albatross nest at low density (approximately 0.0022 nests per m2)56, which could limit spread between breeding individuals. However, non- breeding birds congregate in groups to display and dance57 which may provide opportunities for disease spread. Similar ecological considerations must be made when considering burrow nesting species (such as white-chinned petrel, diving petrel, and prion species), which nest in separated burrow systems and may limit spread. Penguins are also susceptible to HPAIV, and mortality has been observed following infection58. Penguin species nest in high densities (dependent upon species ranging between 0.25 - 1.7 nests per m2)59, 60, and if HPAIV does enter penguin colonies, it could show rapid infection and spread. If the virus does start to cause mass mortality events across penguin colonies, it could signal one of the largest ecological disasters of modern times. Activities within the region are ongoing to track mortality events and autonomous authorities are on high alert to signal the potential for incursions across the broader area.

Genomic analysis of the sequences obtained from South Georgia and the Falkland Islands suggested separate, distinct introductions of the B3.2 HPAIV genotype into the two locations. The B3.2 genotype emerged in early 2022 in the midwestern United States of America as a reassortant formed following coinfection with the original H5N1 that was transmitted from Europe to North America in late 20218 with a North American virus from which the novel genotype emerged, containing the PB2, PB1, NP and NS gene segments of the North American AIVs42. This genotype has been demonstrated to have been introduced into South America four times between October 2022 and March 202310. Analysis of all available full-genome sequences from South America demonstrated that 94% (131 of 140) of H5N1 HPAIV sequences corresponded to this genotype. Given the close geographical proximity of South Georgia and the Falkland Islands to South America, and that wild bird species are known to migrate between the mainland and these islands, it is not surprising that the B3.2 detected as the cause of the disease events. The phylogenetic analyses undertaken demonstrated that the viruses detected in South Georgia and the Falkland Islands shared common ancestors with those detected in mainland South America from late 2022 to early 2023. However, the long branch lengths observed across all gene segments suggest unsampled evolutionary ancestry. There are also only a limited number of sequences deposited in public databases from H5N1 HPAIV detections in South America during summer 2023. Taken together, this highlights the importance of real-time global data sharing as a key tool in understanding the emergence and spread of these viruses. The current lack of publicly available data precludes a conclusive assessment of potential incursion routes substantially more difficult. Multiple disciplines globally continue to monitor the situation in Antarctica to see whether fears of ecological disaster in the region will be realised.

Methods

Virological detection

On the Falkland Islands, initial diagnostic assessment of samples was undertaken at the KEMH Pathology and Food, Water & Environmental Laboratory utilising the QIAamp Viral RNA Mini Kit (Qiagen) and the Oasig OneStep RT-qPCR kit for H5N1 (Genesig). A preliminary diagnosis was made of avian influenza H5N1 infection. Following reports of increasing mortalities and the observation of disease consistent with HPAIV infection in avian and mammalian species in South Georgia, oropharyngeal (OP) and cloacal (C) swabs collected from birds were submitted to the Animal and Plant Health Agency (APHA)-Weybridge for laboratory virological investigation. Total nucleic acid was extracted from all samples61 for testing by a suite of three AIV real-time reverse transcription polymerase chain reaction (rRT-PCR) assays consisting of the Matrix (M)-gene assay for generic influenza A virus detection62; an assay for specific detection of HPAIV H5 clade 2.3.4.4b61 and an N1- specific rRT-PCR to confirm the neuraminidase type63. A positive result was denoted in each case by a Cq value ≤36.0. The samples were also screened for avian paramyxovirus type 1 (APMV-1) by an rRT– PCR assay targeting the large polymerase (L) gene64 where a positive result was denoted by a Cq value ≤37.0. All amplifications were carried out in an AriaMx qPCR System (Agilent, United Kingdom). The OP swabs and the C swabs were separately pooled for attempted virus isolation in 9- to 11-day-old specific pathogen-free (SPF) embryonated fowls’ eggs (EFEs) according to the internationally recognised methods65.

Whole-Genome Sequencing and Phylogenetic Analysis

For whole-genome sequence analysis, the extracted vRNA was converted to double-stranded cDNA and amplified using a one-step RT-PCR using SuperScript III One-Step RT-PCR kit (Thermo Fisher Scientific). The primers used were as follows: Optil-F1 5’-TTACGCGCCAGCAAAAGCAG-3’, Optil-F2 5’-GTTACGCGCCAGCGAAAGCAGG-3’ and Optil-R1 5’-GTTACGCGCCAGTAGAAACAAG-3’ that have been previously described66, 67. PCR products were purified with Agencourt AMPure XP beads (Beckman Coultrer) prior to sequencing library preparation using the Native Barcoding Kit (Oxford Nanopore Technologies) and sequenced using a GridION Mk1 (Oxford Nanopore Technologies) according to manufacturer’s instructions. Assembly of the influenza A viral genomes was performed using a custom in-house pipeline as described previously7 but adapted for nanopore sequence reads. All influenza sequences generated and used in this study are available through the GISAID EpiFlu Database (https://www.gisaid.org). All H5N1 HPAIV clade 2.3.4.4b sequences available in the EpiFlu database between 1st September 2020 and 27th October 2-23 were downloaded to create a sequence dataset. As North America and Europe were over-represented in this dataset, these were sub-sampled to maintain representative sequences using PARNAS68. The remaining dataset was separated by segment and aligned using Mafft v7.52069, and manual trimmed to the open-reading frame using Aliviewversion 1.2670 The trimmed alignments were then used to a infer maximum-likelihood phylogenetic tree using IQ-Tree version 2.2.371 along with ModelFinder7 and 1,000 ultrafast bootstraps72 For the time-resolved and mugration analysis, all HA sequences available from South America, and representative from North America were combined with the sequences from Bird Island and the Falkland Islands and used to infer a maximum-likelihood phylogenetic tree as described above. The resulting tree was then used for ancestral sequence reconstruction and inference of molecular-clock phylogenies using TreeTime73. Phylogenetic reconstruction with discrete trait analysis of the country of origin using the mugration model, was also performed in TreeTime using the default settings. Phylogenetic trees were visualised as described previously72 or using FigTree v1.4.4. Nucleotide identity between sequences was determined as described previously72. Sequences were genotyped according to the USDA schema, using the GenoFLU tool (https://github.com/USDA-VS/GenoFLU)42.

Author contributions

Conceptualisation: ACB, JJ, AB, EMF, ZF; formal analysis: AB, JJ, SMR, KF, ACB, AMPB; investigation: SMR, JLJ, DdS, FB, MB, RH, AMPB, JPD, BM; resources: ACB, JJ, IHB, ZF, EMF; writing—original draft, ACB, JJ, AMPB, SR; writing—review and editing: ACB, JJ, APMB, AB, ZF, EMF, SMR, IHB. All authors have read and agreed to the final version of the manuscript.

Competing interests

The authors declare no competing interests.

Funding statement

This research received no external funding. The testing and generation of the viral sequences was funded by the Department for Environment, Food and Rural Affairs (Defra, UK) and the Devolved Administrations of Scotland and Wales, through the following programmes: SV3400, SV3032, SV3006 and SE2213. This work was also supported by the Biotechnology and Biological Sciences Research Council (BBSRC) and Department for Environment, Food and Rural Affairs (Defra, UK) research initiative ‘FluTrailMap’ [grant number BB/Y007271/1]. This work was also partially supported by KAPPA-FLU HORIZON-CL6-2022-FARM2FORK-02-03 (grant agreement No. 101084171) and Innovate UK (grant number 10085195).

Additional information

Correspondence and requests for materials should be addressed to Ashley.Banyard{at}APHA.gov.uk

Acknowledgements

We would like to thank Thomas Lewis and Vivian Coward from APHA for their help processing these samples and Carrie Gunn from BAS and Vicki Foster from the Government of South Georgia and the South Sandwich Islands. We are grateful for the support and collaboration provided by the Government of South Georgia and the South Sandwich Islands, who have helped to coordinate the response and guidance in response to HPAI at South Georgia. The authors would also like to acknowledge the originating and submitting laboratories of the sequences from GISAID’s EpiFlu Database upon which this research is based, and analyses described in the text. All submitters of the data may be contacted directly via the GISAID website (https://www.gisaid.org). This analysis described in this work was conducted using the Scientific Computing Environment at the Animal and Plant Health Agency.

References

  1. 1.↵
    Adlhoch C, et al. Avian influenza overview February - May 2021. EFSA journal European Food Safety Authority 19, e06951 (2021).
    OpenUrl
  2. 2.↵
    Adlhoch C, et al. Avian influenza overview March - April 2023. EFSA journal European Food Safety Authority 21, e08039 (2023).
    OpenUrl
  3. 3.↵
    Lane JV, et al. High pathogenicity avian influenza (H5N1) in Northern Gannets (Morus bassanus): Global spread, clinical signs and demographic consequences. Ibis n/a.
  4. 4.↵
    Furness RW, et al. Environmental Samples Test Negative for Avian Influenza Virus H5N1 Four Months after Mass Mortality at A Seabird Colony. Pathogens 12, 584 (2023).
  5. 5.↵
    Falchieri M, et al. Shift in HPAI infection dynamics causes significant losses in seabird populations across Great Britain. Veterinary Record 191, 294–296 (2022).
    OpenUrl
  6. 6.↵
    James J, et al. Clade 2.3.4.4b H5N1 high pathogenicity avian influenza virus (HPAIV) from the 2021/22 epizootic is highly duck adapted and poorly adapted to chickens. The Journal of general virology 104, (2023).
  7. 7.↵
    Byrne AMP, et al. Investigating the Genetic Diversity of H5 Avian Influenza Viruses in the United Kingdom from 2020-2022. Microbiology spectrum 11, e0477622 (2023).
    OpenUrl
  8. 8.↵
    Caliendo V, et al. Transatlantic spread of highly pathogenic avian influenza H5N1 by wild birds from Europe to North America in 2021. Scientific Reports 12, 11729 (2022).
  9. 9.↵
    Alkie TN, et al. Recurring Trans-Atlantic Incursion of Clade 2.3.4.4b H5N1 Viruses by Long Distance Migratory Birds from Northern Europe to Canada in 2022/2023. Viruses 15, (2023).
  10. 10.↵
    Leguia M, et al. Highly pathogenic avian influenza A (H5N1) in marine mammals and seabirds in Peru. Nature Communications 14, 5489 (2023).
    OpenUrl
  11. 11.↵
    Marandino A, et al. Spreading of the High-Pathogenicity Avian Influenza (H5N1) Virus of Clade 2.3. 4.4 b into Uruguay. Viruses 15, 1906 (2023).
    OpenUrl
  12. 12.↵
    Jimenez-Bluhm P, et al. Detection and phylogenetic analysis of highly pathogenic A/H5N1 avian influenza clade 2.3. 4.4 b virus in Chile, 2022. Emerging Microbes & Infections, 2220569 (2023).
  13. 13.↵
    Gamarra-Toledo V, et al. Avian flu threatens Neotropical birds. Science 379, 246–246 (2023).
    OpenUrlCrossRef
  14. 14.↵
    Lisovski S, et al. No evidence for highly pathogenic avian influenza virus H5N1 (clade 2.3.4.4b) in the Antarctic region during the austral summer 2022/23. bioRxiv, 2023.2010.2024.563692 (2023).
  15. 15.↵
    Chown SL, Clarke A, Fraser CI, Cary SC, Moon KL, McGeoch MA. The changing form of Antarctic biodiversity. Nature 522, 431–438 (2015).
    OpenUrlCrossRefPubMed
  16. 16.↵
    Frenot Y, et al. Biological invasions in the Antarctic: extent, impacts and implications. Biological reviews 80, 45–72 (2005).
    OpenUrlCrossRefPubMed
  17. 17.↵
    Martin A, Poncet S, Barbraud C, Foster E, Fretwell P, Rothery P. The white-chinned petrel (Procellaria aequinoctialis) on South Georgia: population size, distribution and global significance. Polar Biology 32, 655–661 (2009).
    OpenUrl
  18. 18.↵
    Pardo D, et al. Additive effects of climate and fisheries drive ongoing declines in multiple albatross species. Proceedings of the National Academy of Sciences 114, E10829–E10837 (2017).
    OpenUrlAbstract/FREE Full Text
  19. 19.↵
    Descamps S, et al. Extreme snowstorms lead to large-scale seabird breeding failures in Antarctica. Current Biology 33, R176–R177 (2023).
    OpenUrl
  20. 20.↵
    Steig EJ, Schneider DP, Rutherford SD, Mann ME, Comiso JC, Shindell DT. Warming of the Antarctic ice-sheet surface since the 1957 International Geophysical Year. Nature 457, 459–462 (2009).
    OpenUrlCrossRefGeoRefPubMedWeb of Science
  21. 21.↵
    González-Herrero S, Barriopedro D, Trigo RM, López-Bustins JA, Oliva M. Climate warming amplified the 2020 record-breaking heatwave in the Antarctic Peninsula. Communications Earth & Environment 3, 122 (2022).
  22. 22.↵
    IUCN. The IUCN red list of threatened species. Version 2022-2. IUCN Red List of Threatened Species, (2023).
  23. 23.↵
    Pianka ER. On r-and K-selection. The American Naturalist 104, 592–597 (1970).
    OpenUrlCrossRefWeb of Science
  24. 24.↵
    Camphuysen C, Gear S, Furness R. Avian influenza leads to mass mortality of adult Great Skuas in Foula in summer 2022. Scott Birds 42, 312–323 (2022).
    OpenUrl
  25. 25.↵
    Banyard AC, et al. Detection of Highly Pathogenic Avian Influenza Virus H5N1 Clade 2.3.4.4b in Great Skuas: A Species of Conservation Concern in Great Britain. Viruses 14, (2022).
  26. 26.↵
    Costa ES, et al. Antarctic and sub-Antarctic seabirds in South America: a review. Oecologia Australis 15, 59–68 (2011).
    OpenUrl
  27. 27.↵
    Meagan Dewar RETV, Thierry Boulinier, Craig Cary, Augustin Clessin, Amandine Gamble, Rachael Gray, Wray Grimaldi, Tom Hart, Virginia Morandini, Soledad Leonardi, Marcela Uhart, Jane Younger, Michelle Wille. Biological Risk Assessment of Highly Pathogenic Avian Influenza in the Southern Ocean.). Scientific Committee on Antarctic Research (2023).
  28. 28.↵
    Baumeister E, et al. Serological evidences of influenza A virus infection in Antarctica migratory birds. In: International Congress Series). Elsevier (2004).
  29. 29.↵
    de Seixas MMM, et al. H6N8 avian influenza virus in Antarctic seabirds demonstrates connectivity between South America and Antarctica. Transboundary and emerging diseases 69, e3436–e3446 (2022).
    OpenUrl
  30. 30.↵
    Hurt AC, et al. Evidence for the Introduction, Reassortment, and Persistence of Diverse Influenza A Viruses in Antarctica. Journal of Virology 90, 9674–9682 (2016).
    OpenUrlAbstract/FREE Full Text
  31. 31.↵
    Zamora G, et al. Scavengers as Prospective Sentinels of Viral Diversity: the Snowy Sheathbill Virome as a Potential Tool for Monitoring Virus Circulation, Lessons from Two Antarctic Expeditions. Microbiology spectrum 11, e03302–03322 (2023).
    OpenUrl
  32. 32.↵
    de Souza Petersen E, et al. First detection of avian influenza virus (H4N7) in Giant Petrel monitored by geolocators in the Antarctic region. Marine Biology 164, 1–9 (2017).
    OpenUrlCrossRef
  33. 33.↵
    Boulinier T. Avian influenza spread and seabird movements between colonies. Trends in Ecology & Evolution, (2023).
  34. 34.↵
    Gittins O, et al. Serological and molecular surveys of influenza A viruses in Antarctic and sub-Antarctic wild birds. Antarctic Science 32, 15–20 (2020).
    OpenUrl
  35. 35.↵
    Wallensten A, et al. Mounting evidence for the presence of influenza A virus in the avifauna of the Antarctic region. Antarctic Science 18, 353–356 (2006).
    OpenUrl
  36. 36.↵
    Morgan I, Westbury H. Virological studies of Adelie penguins (Pygoscelis adeliae) in Antarctica. Avian Diseases, 1019-1026 (1981).
  37. 37.↵
    Austin F, Webster R. Evidence of ortho-and paramyxoviruses in fauna from Antarctica. Journal of Wildlife Diseases 29, 568–571 (1993).
    OpenUrlCrossRefPubMedWeb of Science
  38. 38.↵
    Barriga G, et al. Avian Influenza Virus H5 Strain with North American and Eurasian Lineage Genes in an Antarctic Penguin. Emerging Infectious Disease journal 22, 2221 (2016).
    OpenUrl
  39. 39.↵
    Ogrzewalska M, et al. Influenza A (H11N2) Virus Detection in Fecal Samples from Adélie (Pygoscelis adeliae) and Chinstrap (Pygoscelis antarcticus) Penguins, Penguin Island, Antarctica. Microbiology spectrum 10, e01427–01422 (2022).
    OpenUrl
  40. 40.↵
    Hurt AC, et al. Detection of evolutionarily distinct avian influenza A viruses in Antarctica. MBio 5, doi:10.1128/mbio.01098-01014 (2014).
    OpenUrlCrossRef
  41. 41.↵
    Dewar M, et al. The Risk of Avian Influenza in the Southern Ocean: A practical guide. (2022).
  42. 42.↵
    Youk S, et al. H5N1 highly pathogenic avian influenza clade 2.3.4.4b in wild and domestic birds: Introductions into the United States and reassortments, December 2021–April 2022. Virology 587, 109860 (2023).
    OpenUrl
  43. 43.↵
    Wolfaardt A, Christie D. Guidelines for the implementation of the Agreement on the Conservation of Albatrosses and Petrels (ACAP) at South Georgia and the South Sandwich Islands. Government of South Georgia and the South Sanwich Islands, Stanley, Falkland Islands, (2010).
  44. 44.↵
    Tancell C, Sutherland WJ, Phillips RA. Marine spatial planning for the conservation of albatrosses and large petrels breeding at South Georgia. Biological Conservation 198, 165–176 (2016).
    OpenUrl
  45. 45.↵
    Hogg OT, Barnes DK, Griffiths HJ. Highly diverse, poorly studied and uniquely threatened by climate change: an assessment of marine biodiversity on South Georgia’s continental shelf. PloS one 6, e19795 (2011).
    OpenUrlCrossRefPubMed
  46. 46.↵
    Clarke A, Croxall JP, Poncet S, Martin AR, Burton R. Important bird areas: South Georgia. British Birds 105, 118–144 (2012).
    OpenUrl
  47. 47.↵
    Wakefield ED, et al. Space Partitioning Without Territoriality in Gannets. Science 341, 68–70 (2013).
    OpenUrlAbstract/FREE Full Text
  48. 48.↵
    Votier SC, Grecian WJ, Patrick S, Newton J. Inter-colony movements, at-sea behaviour and foraging in an immature seabird: results from GPS-PPT tracking, radio-tracking and stable isotope analysis. Marine biology 158, 355–362 (2011).
    OpenUrlCrossRefWeb of Science
  49. 49.↵
    Jeglinski J, et al. HPAIV outbreak triggers long-distance movements in breeding Northern gannets--implications for disease spread. (2023).
  50. 50.↵
    Croxall JP, Silk JR, Phillips RA, Afanasyev V, Briggs DR. Global circumnavigations: tracking year-round ranges of nonbreeding albatrosses. Science 307, 249–250 (2005).
    OpenUrlAbstract/FREE Full Text
  51. 51.↵
    Phillips RA, Silk JRD, Croxall JP, Afanasyev V. Year-round distribution of white-chinned petrels from South Georgia: Relationships with oceanography and fisheries. Biological Conservation 129, 336–347 (2006).
    OpenUrlCrossRefWeb of Science
  52. 52.↵
    Techow N, et al. Speciation and phylogeography of giant petrels Macronectes. Molecular Phylogenetics and Evolution 54, 472–487 (2010).
    OpenUrl
  53. 53.↵
    Postel A, et al. Infections with highly pathogenic avian influenza A virus (HPAIV) H5N8 in harbor seals at the German North Sea coast, 2021. Emerging Microbes & Infections 11, 725–729 (2022).
    OpenUrl
  54. 54.↵
    Mirolo M, et al. Highly pathogenic avian influenza A virus (HPAIV) H5N1 infection in two European grey seals (Halichoerus grypus) with encephalitis. Emerging Microbes & Infections 12, e2257810 (2023).
    OpenUrl
  55. 55.↵
    Grémillet D, et al. Strong breeding colony fidelity in northern gannets following high pathogenicity avian influenza virus (HPAIV) outbreak. Biological Conservation 286, 110269 (2023).
  56. 56.↵
    Underhill L, Petersen S, Cooper J. Nest densities of the wandering albatross Diomedea exulans at the Prince Edward Islands, estimated using GPS. African Journal of Marine Science 25, 529–535 (2003).
    OpenUrl
  57. 57.↵
    Jouventin P, Lequette B. The dance of the Wandering Albatross Diomedea exulans. Emu- Austral Ornithology 90, 123–131 (1990).
    OpenUrl
  58. 58.↵
    Abolnik C, et al. The Molecular Epidemiology of Clade 2.3.4.4B H5N1 High Pathogenicity Avian Influenza in Southern Africa, 2021-2022. Viruses 15, (2023).
  59. 59.↵
    Crawford R, Cooper J, Dyer B. Population of the macaroni penguin Eudyptes chrysolophus at Marion Island, 1994/95–2002/03, with information on breeding and diet. African Journal of Marine Science 25, 475–486 (2003).
    OpenUrl
  60. 60.↵
    Quintana R, Cirelli V. Breeding dynamics of a gentoo penguin Pygoscelis papua population at Cierva Point, Antarctic Peninsula. Marine Ornithology 28, 29–35 (2000).
    OpenUrl
  61. 61.↵
    James J, et al. Rapid and sensitive detection of high pathogenicity Eurasian clade 2.3.4.4b avian influenza viruses in wild birds and poultry. Journal of Virological Methods 301, 114454 (2022).
    OpenUrlCrossRef
  62. 62.↵
    Spackman E, et al. Development of a Real-Time Reverse Transcriptase PCR Assay for Type A Influenza Virus and the Avian H5 and H7 Hemagglutinin Subtypes. Journal of Clinical Microbiology 40, 3256–3260 (2002).
    OpenUrlAbstract/FREE Full Text
  63. 63.↵
    Payungporn S, et al. Single step multiplex real-time RT-PCR for H5N1 influenza A virus detection. Journal of Virological Methods 131, 143–147 (2006).
    OpenUrlCrossRefPubMedWeb of Science
  64. 64.↵
    Sutton DA, et al. Development of an avian avulavirus 1 (AAvV-1) L-gene real-time RT-PCR assay using minor groove binding probes for application as a routine diagnostic tool. Journal of Virological Methods 265, 9–14 (2019).
    OpenUrl
  65. 65.↵
    World Organisation for Animal Health (WOAH). Terrestrial Manual: Avian influenza (infection with avian influenza viruses).) (2019).
  66. 66.↵
    Chrzastek K, et al. Use of Sequence-Independent, Single-Primer-Amplification (SISPA) for rapid detection, identification, and characterization of avian RNA viruses. Virology 509, 159–166 (2017).
    OpenUrl
  67. 67.↵
    Leyson C, et al. Pathogenicity and genomic changes of a 2016 European H5N8 highly pathogenic avian influenza virus (clade 2.3.4.4) in experimentally infected mallards and chickens. Virology 537, 172–185 (2019).
    OpenUrl
  68. 68.↵
    Markin A, Wagle S, Grover S, Vincent Baker AL, Eulenstein O, Anderson TK. PARNAS: Objectively Selecting the Most Representative Taxa on a Phylogeny. Systematic Biology 72, 1052–1063 (2023).
    OpenUrl
  69. 69.↵
    Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular biology and evolution 30, 772–780 (2013).
    OpenUrlCrossRefPubMedWeb of Science
  70. 70.↵
    Larsson A. AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30, 3276–3278 (2014).
    OpenUrlCrossRefPubMed
  71. 71.↵
    Minh BQ, et al. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Molecular biology and evolution 37, 1530–1534 (2020).
    OpenUrlCrossRefPubMed
  72. 72.↵
    Lean FZX, et al. Subclinical hepatitis E virus infection in laboratory ferrets in the UK. The Journal of general virology 103, (2022).
  73. 73.↵
    Sagulenko P, Puller V, Neher RA. TreeTime: Maximum-likelihood phylodynamic analysis. Virus evolution 4, vex042 (2018).
Back to top
Posted November 24, 2023.
Download PDF

Supplementary Material

Email
Detection and spread of high pathogenicity avian influenza virus H5N1 in the Antarctic Region
Ashley Bennison, Alexander M. P. Byrne, Scott M. Reid, Joshua G. Lynton-Jenkins, Benjamin Mollett, Dilhani De Sliva, Jacob Peers-Dent, Kim Finlayson, Rosamund Hall, Freya Blockley, Marcia Blyth, Marco Falchieri, Zoe Fowler, Elaine M. Fitzcharles, Ian H. Brown, Joe James, Ashley C. Banyard
bioRxiv 2023.11.23.568045; doi: https://doi.org/10.1101/2023.11.23.568045
Twitter logo Facebook logo LinkedIn logo Mendeley logo
Citation Tools

Subject Area