Pinnipeds and avian influenza: a global timeline and review of research on the impact of highly pathogenic avian influenza on pinniped populations with particular reference to the endangered Caspian seal (Pusa caspica)

Abstract

This study reviews chronologically the international scientific and health management literature and resources relating to impacts of highly pathogenic avian influenza (HPAI) viruses on pinnipeds in order to reinforce strategies for the conservation of the endangered Caspian seal (Pusa caspica), currently under threat from the HPAI H5N1 subtype transmitted from infected avifauna which share its haul-out habitats. Many cases of mass pinniped deaths globally have occurred from HPAI spill-overs, and are attributed to infected sympatric aquatic avifauna. As the seasonal migrations of Caspian seals provide occasions for contact with viruses from infected migratory aquatic birds in many locations around the Caspian Sea, this poses a great challenge to seal conservation. These are thus critical locations for the surveillance of highly pathogenic influenza A viruses, whose future reassortments may present a pandemic threat to humans.

Keywords: Caspian Sea nature conservation; Caspian seal; HPAI H5N1; avian influenza viruses; marine mammals; phylogenetics; pinnipeds; surveillance.

Figure 1

Graph plotting annual numbers of Caspian seals harvested between 1867 and 2020 (none were culled after 2000). Compiled from: FAO Fishsta+; Caspian Environment Programme, Transboundary Analysis Revisit (2007); and Härkönen et al. (2012). The latter assessed significantly less seals born in most of these years than were harvested.

Figure 2

Reported HPAI A(H5N1) animal outbreaks reported to the World Organization for Animal Health (WOAH), January 2022-June 2023. After: Australian Bureau of Statistics, Geonames, Microsoft, Navinfo, Open Street Map, Tom Tom, Zenrin.

Figure 3

July 2023 map of global distribution of AIV with zoonotic potential (including H5Nx HPAI viruses) since 1 October 2022. Food and Agricultural Organization of the United Nations. These are outbreaks in animals officially reported since the previous update (22 HPAI subtypes: H5 (untyped) (53), H5N1 (625), H5N5 (2), H5N6 (1) and H7 (4). After FAO: https://www.fao.org/animal-health/situation-updates/global-aiv-with-zoonotic-potential/en.

Figure 4

Map showing the hub of a number of migratory flyways used by aquatic birds in the northern area of the Caspian Sea where Maliy Zhemchuzhniy Island is located. Derived from: Google Earth & Vilkov, 2016b. https://doi.org/10.1134/S199542551603015X.

Figure 5

Southern tip of Maliy Zhemchuzhniy Island, northern Caspian Sea, Russia, showing Caspian seals in proximity to aquatic birds and their breeding colonies (great black-headed gulls, Caspian gulls and Caspian terns). Photo: ASNBR, 11 April 2020.

Figure 6

Northern tip of Maliy Zhemchuzhniy Island, northern Caspian Sea, Russia, showing Caspian seals in close proximity to aquatic birds (great cormorants, Caspian gulls and Caspian terns). Photo: ASNBR, 11 April 2020.

Figure 7

Maximum-likelihood phylogenetic tree of the hemagglutinin segment. Circles indicate HPAI H5N1 virus strains detected in birds on Maliy Zhemchuzhniy Island. Rhombuses indicate H5Nx viruses of clade 2.3.4.4b isolated from mammals (including marine mammals). The multiple alignment was performed using MUSCLE. Maximum-likelihood phylogenetic analysis was generated and visualized by MEGA5 using the general time-reversible nucleotide substitution model. Bootstrap support values were generated using 500 rapid bootstrap replicates.

Figure 8

HPAI virus infections in wild birds’ categories 28 April 2023 – 23 June 2023. After European Food Safety Authority, European Centre for Disease Prevention and Control, European Union Reference Laboratory for Avian Influenza, Avian influenza overview April – June 2023.

Figure 9

HPAI subtype detections in wild birds 29 April 2023 – 23 June 2023. After European Food Safety Authority, European Centre for Disease Prevention and Control, European Union Reference Laboratory for Avian Influenza, Avian influenza overview April – June 2023.

Figure 10

Steller sea lions (a threatened species) and aquatic birds (mainly glaucous-winged gulls – a vector for AIV) in typical close habitat association on Whale Rocks, WA, USA. Used by permission of the San Juan Preservation Trust (sjpt.org). Photo by Stephanie Colony.

Figure 11

Peruvian pelican stricken with HPAI H5N1 on the Peruvian coast. South American sea lions in the background. February 2023. After: https://phys.org/news/2023-02-peru-hundreds-sea-lion-deaths.html.

Figure 12

South American sea lions and aquatic birds (rock cormorants and Dominican or dolphin gulls) sharing the same habitat and in close association. Beagle Channel, Tierra del Fuego, Argentina. October 2007. Photo: gailhampshire from Cradley, Malvern, U.K, CC BY 2.0 https://creativecommons.org/licenses/by/2.0 via Wikimedia Commons.

Figure 13

Locations of migratory aquatic avifauna stop-over sites proposed along the Caspian Sea littoral for the ViEW (Virus Early Warning) transboundary surveillance program for AIV. After: Petherbridge et al. (2022).

Figure 14

Locations of principal Caspian seal molting and haul out habitat zones in the Caspian Sea as mapped by the IUCN Marine Mammals Protected Areas (IMMA) Task Force in 2016. These are also seasonal stop-over sites for migratory aquatic avifauna. They are proposed for the ViEW (Virus Early Warning) transboundary surveillance program for AIV in seals.