Outbreak dynamics of high pathogenicity avian influenza virus H5N1, clade 2.3.4.4b euBB, in black-headed gulls and common terns in Germany in 2023.

Ulrich Knief1 Ann Kathrin Ahrens2 Valerie Allendorf2 Carla J Behringer3 Justine Bertram4 Sandra Bouwhuis4 Wolfgang Fiedler5 Anja Globig2 Anne Günther2 Christof Herrmann6 Sascha Knauf2,7 Dominik Marchowski8 Simon Piro6 Anne Pohlmann2 Robert E Rollins4 Christoph Staubach2 Timm Harder2
Affiliations 8 institutions
  1. Evolutionary Biology and Ecology, University of Freiburg, Institute of Biology I (Zoology), Freiburg, Germany.
  2. Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Greifswald-Insel Riems, Germany.
  3. Fakultät für Biologie, Universität Innsbruck, Innsbruck, Austria.
  4. Institute of Avian Research, Wilhelmshaven, Germany.
  5. Max Planck Institute of Animal Behavior, Radolfzell, Germany.
  6. Agency for Environment, Nature Conservation, and Geology Mecklenburg-Western Pomerania, Hiddensee Bird Ringing Scheme, Güstrow, Germany.
  7. Faculty of Veterinary Medicine, Justus Liebig University, Giessen, Germany.
  8. Ornithological Station, Museum and Institute of Zoology, Polish Academy of Sciences, Gdańsk, Poland.

Abstract

Since the winter of 2022/23, the high pathogenicity avian influenza virus (HPAIV) H5N1 clade 2.3.4.4b, genotype euBB, has caused extensive mortality among wild birds. This genotype emerged in France in spring 2022 through reassortment between a gull-adapted low-pathogenicity virus and HPAIV H5N1. Here, we investigated the spread, virus-related mortality, and population-level impact of genotype euBB in black-headed gulls (Chroicocephalus ridibundus) and common terns (Sterna hirundo) in Germany using phylogeographic analyses, ringing data, and information on spatiotemporal outbreak patterns. Transmission into German breeding colonies involved multiple independent incursions, likely associated with black-headed gulls returning from their wintering grounds in the Netherlands, Belgium, and France. It spilled over into common terns, and led to high adult mortality in both species in 2023 (at least 8,137 black-headed gulls and 614 common terns; >3% of the breeding population), followed by significant breeding pair declines in 2024 (-16% in black-headed gulls, -6% in common terns). Increased immunity, at least in common terns, may have contributed to the apparent subsequent fade-out of genotype euBB. These findings highlight how integrating ornithological, epidemiological, and virological data can aid our understanding of viral transmission routes and population-level impacts, while also stressing that HPAIV should be added to the growing list of pressures on seabirds, a group that was already the most threatened among all bird taxa globally.RESEARCH HIGHLIGHTS Multiple independent HPAIV H5N1 euBB incursions occurred in Germany in 2023.HPAIV H5N1 euBB caused mass mortality in black-headed gulls and common terns.Outbreaks reduced gull and tern breeding populations by 16% and 6%, respectively.Rising H5-seroprevalence in terns may have contributed to the fade-out of genotype euBB.

Supporting text Virus Host Location
active surveillance 3 H5N1 82 HPAI 19 mass mortality 2 population impact 1 seabirds 4

Evidence records

5 total
Zoonotic Surveillance
1 records · 1 evidence types
Evidence type
1 records
OVE10986
Key finding

Rising H5-seroprevalence was observed in common terns, indicating increased antibody-based immunity to HPAIV H5N1 genotype euBB.

Virus
Host
Location
Not specified
Supporting text

RESEARCH HIGHLIGHTS: Rising H5-seroprevalence in terns may have contributed to the fade-out of genotype euBB.

Method
serological assay | antibody detection
Transmission Evidence
2 records · 2 evidence types
Evidence type
1 records
OVE10984
Key finding

An outbreak of high pathogenicity avian influenza virus H5N1 clade 2.3.4.4b genotype euBB in 2023 caused extensive mortality among black-headed gulls and spilled over into common terns in Germany.

Virus
Host
Location
Supporting text

Here, we investigated the spread, virus-related mortality, and population-level impact of genotype euBB in black-headed gulls (Chroicocephalus ridibundus) and common terns (Sterna hirundo) in Germany ... It spilled over into common terns, and led to high adult mortality in both species in 2023 (at least 8,137 black-headed gulls and 614 common terns; >3% of the breeding population).

Method
phylogeographic analyses | ringing data | spatiotemporal outbreak pattern investigation
Transmission direction
animal-to-animal
Geographic raw
Germany
Country inferred
DEU
Outbreak setting
wild bird breeding colonies
Outbreak time
2023
Outbreak scale
at least 8,137 black-headed gulls and 614 common terns; >3% of the breeding population
Evidence type
1 records
OVE10985
Key finding

High pathogenicity avian influenza virus H5N1 clade 2.3.4.4b genotype euBB spilled over from black-headed gulls into common terns during breeding colony outbreaks in Germany in 2023.

Virus
Host
Location
Supporting text

Transmission into German breeding colonies involved multiple independent incursions, likely associated with black-headed gulls returning from their wintering grounds in the Netherlands, Belgium, and France. It spilled over into common terns, and led to high adult mortality in both species in 2023.

Method
phylogeographic analyses | ringing data | spatiotemporal outbreak pattern analysis
Study design
field outbreak investigation with phylogeographic and epidemiological analysis
Transmission direction
animal-to-animal
Geographic raw
Germany
Genomic Evolution
2 records · 2 evidence types
Evidence type
1 records
OVE10983
Key finding

The high pathogenicity avian influenza virus H5N1 clade 2.3.4.4b genotype euBB originated in France in 2022 through reassortment between a gull-adapted low-pathogenicity influenza virus and HPAIV H5N1.

Virus
Host
Not specified
Location
Not specified
Supporting text

This genotype emerged in France in spring 2022 through reassortment between a gull-adapted low-pathogenicity virus and HPAIV H5N1.

Event type
reassortment
Evidence type
1 records
OVE10987
Key finding

Phylogeographic analyses showed that high pathogenicity avian influenza virus H5N1 clade 2.3.4.4b genotype euBB underwent multiple independent incursions into Germany in 2023.

Virus
Host
Location
Not specified
Supporting text

Here, we investigated the spread, virus-related mortality, and population-level impact of genotype euBB in black-headed gulls (<i>Chroicocephalus ridibundus</i>) and common terns (<i>Sterna hirundo</i>) in Germany using phylogeographic analyses, ringing data, and information on spatiotemporal outbreak patterns. Transmission into German breeding colonies involved multiple independent incursions, likely associated with black-headed gulls returning from their wintering grounds in the Netherlands, Belgium, and France.

Analysis methods
phylogeographic analyses