Waterfowl Spring Migratory Behavior and Avian Influenza Transmission Risk in the Changing Landscape of the East Asian-Australasian Flyway

Abstract

Avian influenza has advanced from a regional concern to a global health issue with significant economic, trade, and public health implications. Wild birds, particularly waterfowl (Anseriformes), are known reservoirs for low-pathogenic avian influenza viruses (AIV) and recent studies have shown their potential in the spread of highly pathogenic forms of virus. East Asia remains an epicenter for the emergence of novel strains of AIV, however, information on movement ecology of waterfowl, and subsequently a clearer understanding of disease transmission risks in this region has been greatly lacking. To address this, we marked two species of wild waterfowl, northern pintail (Anas acuta) and Eurasian wigeon (Anas penelope), with satellite transmitters on their wintering grounds in Hong Kong, China to study the northward spring migration in the East Asian-Australasian Flyway in relation to disease transmission factors. Northern pintail were found to initiate migration 42 days earlier, travel 2,150 km farther, and perform 4.4 more stopovers than Eurasian wigeon. We found both species used similar stopover locations including areas along the Yangtze River near Shanghai, Bohai Bay and Korea Bay in rapidly developing regions of the Yellow Sea, and the Sea of Okhotsk where the species appeared to funnel through a migratory bottleneck. Both species appeared to exhibit strong habitat selection for rice paddies during migration stopovers, a habitat preference which has the potential to influence risks of AIV outbreaks as rapid land use and land cover changes occur throughout China. Both species had greatest association with H5N1 outbreaks during the early stages of migration when they were at lower latitudes. While Eurasian wigeon were not associated with outbreaks after the mean date of wintering ground departures, northern pintail were associated with outbreaks until the majority of individuals departed from the Yellow Sea, a migratory stopover location. Our results show species-level differences in migration timing and behavior for these common and widespread species, demonstrating the need to consider their unique temporal and spatial movement ecology when incorporating wild birds into AIV risk modeling and management.

Continental‐scale dynamics of avian influenza in U.S. waterfowl are driven by demography, migration, and temperature

“…Our work also quantifies the movement of birds in a network context and provides a data‐driven assessment of multiple scales of the migration process. Most work on the role of bird movements in the spread of AIV has focused on the inferred movement of birds between two to a few locations (Hoye et al 2011, Hill et al 2012, Hill et al 2012, Hill et al 2016) or the role of migratory flyways (Fourment et al 2017; but not always, Tian et al 2015, Sullivan et al 2018). Migratory flyways represent common migratory paths and are presumed to represent populations that can be discretely managed (Lincoln 1935).…”

“…Third, the contact and mixing patterns among wild birds at local, intermediate, and continental scales generate a contact network that may influence the spatial and temporal distribution of AIV. For example, bird movement into an area, the migration of birds within biological flyways, and continental‐scale mixing among flyways may all mediate infection by influencing transmission among aggregated birds and virus introduction (Hill et al 2012, 2016, Tian et al 2015, Sullivan et al 2018). Few studies have monitored waterfowl movement beyond pairwise connections in order to relate the dynamic network generated through migration to AIV dynamics.…”

Population genomics of louping ill virus provide new insights into the evolution of tick-borne flaviviruses

“…Alternatively, LIV may have been introduced to Turkmenistan and Russia via the transport of ticks by migratory birds. The transport of tick-borne pathogens between countries by birds has been well documented [ 98 – 100 ], as is the long-distance dispersal of avian influenza viruses by migratory waterfowl [ 101 – 103 ]. However, there are no direct migratory links between central/northeast Eurasia and the UK [ 104 ] and in order to transport LIV, birds must reside in environments where LIV is prevalent, such as upland moors, long enough for infected ticks to attach.…”

Waterfowl occurrence and residence time as indicators of H5 and H7 avian influenza in North American Poultry

“…Mapped AIP probabilities predicted by joint-model (Model5). Weeks 7,15,18,23,33, and 51 of the year are labeled as A through F respectively. Color coding and legend reflect relative probability (0.00-1.00) of H5 or H7 occurrence in North American Poultry with darker colors signifying increased likelihood.…”

“…To assess the potential role of migratory waterfowl in transporting HPAI viruses throughout central and eastern Asia, several studies have examined the spatial and temporal overlap of waterfowl movement trajectories or utilization distributions with disease occurrence locations, poultry facilities, and key waterfowl habitats 3,[29][30][31][32][33] , however, there are a lack of comparable waterfowl movement studies investigating associations with avian influenza outbreaks in the Western Hemisphere. Indeed, there is a recognized need for new methods and tools to help quantify the dynamic interaction between wild bird hosts and commercial poultry in North America [34][35][36] .…”