Avian raptors are indicator species and victims of high pathogenicity avian influenza virus HPAIV H5N1 (clade 2.3.4.4b) in Germany

Abstract

Transition of highly pathogenic clade 2.3.4.4b H5 avian influenza virus (HPAIV) from epizootic to enzootic status in Northern European countries was associated with severe losses and even mass mortalities among various wild bird species. Both avian and mammalian raptors hunting infected debilitated birds or scavenging on virus-contaminated avian carcasses contracted HPAIV infection. This precarious pathogen-prey-predator relation further worsened when in 2021 and 2022 outbreaks in Germany overlapped with the hatching season of avian raptor species. Retro- and prospective surveillance revealed avian raptors as important indicators of HPAIV and its genetic diversity on the one hand. On the other hand, their role as victims of HPAIV is stipulated. The first case of an HPAIV H5N1-related death of a white-tailed sea eagle (Haliaeetus albicilla; WTSE) hatch in Germany, 2021, followed by several such cases in 2022, and a low overall seropositivity rate of 5.0-7.9% among WTSE nestlings, raised fears of a serious negative impact on reproduction rates of WTSEs and other birds of prey when HPAIV becomes enzootic in an ecosystem. However, comparably stable breeding success of WTSE in the study area in 2022 and a potentially evolving natural immunity raises hope for a less severe long-term impact.

Keywords: Haliaeetus albicilla; Highly pathogenic avian influenza virus H5N1; Maternal immunity; Nestling; White-tailed sea eagle; Wild bird surveillance.

Fig. 1

Overview of individual avian raptors sampled within the retrospective (A) or prospective (B) surveillance approach in this study, including additional information on age cohorts and scavenging behavior. Abbreviations of the German federal states: BB—Brandenburg; MWP – Mecklenburg-Western Pomerania.

Fig. 2

Numbers of raptors screened for influenza A viruses (IAV) and testing positive for gs/GD highly pathogenic avian influenza viruses (HPAIV). The proportion of HPAIV-positive birds is given for the retrospective surveillance across the whole of Germany between 2016–2022 (A) and nestlings and non-nestlings (B), sampled within the prospective-regional sampling approach in Mecklenburg-Western Pomerania (MWP), a Federal State in the Northeast of Germany (2021 and 2022).

Fig. 3

Distribution of relative viral load (low Cq values indicate high viral loads) in HPAIV H5N1-positive white-tailed sea eagles, screened by RT-qPCR. The results are presented per sample matrix (oropharyngeal or cloacal swab or organ) and individual bird. Individuals are assigned numbers and letters, where numbers indicate a specific nest and letters the different nestling therein. Samples taken from individuals alive are shown in blue, samples taken from dead nestlings are shown in red.

Fig. 4

HPAIV H5 genotype variation in Germany. Between calendar week 44 in 2020 and 48 in 2022, 33 distinct genotypes were found in total (unique colour codes, upper panel). Of these, eight were found in avian raptors (highlighted), and additional information on their temporal occurrence and distribution, raptor host species (groups) and other affected hosts is summarized. Ger-11–21-N1.4 is shaded in grey emphasizing that it is the only genotype found exclusively in a raptor host. Abbreviations of the German federal states: BB—Brandenburg; MWP – Mecklenburg-Western Pomerania; NI—Lower Saxony; NW – North Rhine-Westphalia; SH—Schleswig–Holstein.

Fig. 5

Serological results of samples retrieved from avian raptors. The results are shown in percent inhibition values measured by competition ELISA to detect antibodies against the nucleoprotein (NP, black symbols, grey indeterminate range 45–50%; positive < 45%). NP-positive sera were further tested against the hemagglutinin H5 (H5, red symbols, pinkish indeterminate range 50–60%; positive < 50%). (A) Serological status of individuals sampled within the prospective-regional surveillance approach in Mecklenburg-Western Pomerania (MWP), Germany in 2021 and 2022. The data are grouped per species and age, indicating mean and standard error of the mean. Data points for certain individuals are highlighted by specific numbers; numbers correspond to listings in Supplementary Tables 1–3. P-value < 0.05 is confirming significant differences comparing NP-positive findings in white-tailed sea eagle (WTSE) nestlings (n(positive) = 8; n(non-positive) = 108) and nestlings of all other raptor species (n(positive) = 0; n(non-positive) = 69) via the Fisher-test. (B) Serological status of WTSE analyzed retrospectively, based on left-over material from other research projects (2006–2021) or obtained within a prospective targeted surveillance approach in MWP, Germany (2021–2022). The data are stratified by year of sample origin and by age cohort indicating mean and standard error of the mean.

Fig. 6

Number of breeding pairs (A) and breeding success rate (B) of white-tailed sea eagles in two selected regions of the federal German state of Mecklenburg-Western Pomerania (MWP; Isle of Rügen and Isle of Usedom) and in total MWP, 2002–2022 (Table S8). Grey plots summarize the scenarios for 2002–2021, while red dots indicate the data for 2022 when HPAIV H5N1 of clade 2.3.4.4b was enzootically prevalent in those regions.