Influenza A Viruses in Ruddy Turnstones (Arenaria interpres); Connecting Wintering and Migratory Sites with an Ecological Hotspot at Delaware Bay

Abstract

Each May for over three decades, avian influenza A viruses (IAVs) have been isolated from shorebirds and gulls (order Charadriiformes) at Delaware Bay (DE Bay), USA, which is a critical stopover site for shorebirds on their spring migration to arctic breeding grounds. At DE Bay, most isolates have been recovered from ruddy turnstones (Arenaria interpres), but it is unknown if this species is involved in either the maintenance or movement of these viruses outside of this site. We collected and tested fecal samples from 2823 ruddy turnstones in Florida and Georgia in the southeastern United States during four winter/spring sample periods—2010, 2011, 2012, and 2013—and during the winters of 2014/2015 and 2015/2016. Twenty-five low pathogenicity IAVs were recovered representing five subtypes (H3N4, H3N8, H5N9, H6N1, and H12N2). Many of these subtypes matched those recovered at DE Bay during the previous year or that year’s migratory cycle, suggesting that IAVs present on these southern wintering areas represent a source of virus introduction to DE Bay via migrating ruddy turnstones. Analyses of all IAV gene segments of H5N9 and H6N1 viruses recovered from ruddy turnstones at DE Bay during May 2012 and from the southeast during the spring of 2012 revealed a high level of genetic relatedness at the nucleotide level, suggesting that migrating ruddy turnstones move IAVs from wintering grounds to the DE Bay ecosystem.

Maintenance and dissemination of avian-origin influenza A virus within the northern Atlantic Flyway of North America

“…Despite banding data for waterfowl providing empirical evidence of migratory connectivity between sampling sites in Maine and Maryland, we did not find evidence of whole genome constellation dispersal of IAV by wild birds between these two states. These results are not unusual when compared to other studies [ 58 , 62 ] and possible, non-mutually exclusive explanations for our findings include: (1) viral dispersal of genome constellations is relatively rare and our sample was insufficient for detection of such an event, (2) Maine is likely one of multiple migratory connections (i.e. source populations of IAV) for the waterfowl sampled in Maryland, and (3) rapid accumulation of point mutations and widespread reassortment within the wild bird reservoir leads to highly transient genome constellations of IAVs.…”

“…source populations of IAV) for the waterfowl sampled in Maryland, and (3) rapid accumulation of point mutations and widespread reassortment within the wild bird reservoir leads to highly transient genome constellations of IAVs. These findings of direct spatial migratory connectivity of avian hosts, lack of detection of nearly identical IAV genomes at spatially distant locations within a flyway, and evidence for dispersal of viral gene segments between northern and southern locations used by migratory birds are congruent with what has been reported for shorebirds sampled within the same flyway [ 58 ] and waterfowl sampled to the west in the Mississippi Flyway [ 62 ].…”

“…Such virus exchange has proven ecologically and economically relevant as exemplified by frequent HPAI H5N1 detections in North America beginning in late 2021 [ 39 , 41 ]. Although there have been studies that provide information on virus subtypes and prevalence for waterfowl within the Atlantic Flyway [ 53 – 56 ], there are fewer studies that investigate viral genetic persistence or dispersal [ 57 , 58 ] which can help elucidate patterns in virus transport to new areas via wild birds. One exception is a long-standing IAV surveillance effort in the U.S. that focuses on shorebirds, mainly ruddy turnstones (Arenaria interpres) , that migrate thru Delaware Bay, coinciding with mass numbers of breeding horse-shoe crabs ( Limulus polyphemus ) [ 58 – 60 ].…”

“…Although there have been studies that provide information on virus subtypes and prevalence for waterfowl within the Atlantic Flyway [ 53 – 56 ], there are fewer studies that investigate viral genetic persistence or dispersal [ 57 , 58 ] which can help elucidate patterns in virus transport to new areas via wild birds. One exception is a long-standing IAV surveillance effort in the U.S. that focuses on shorebirds, mainly ruddy turnstones (Arenaria interpres) , that migrate thru Delaware Bay, coinciding with mass numbers of breeding horse-shoe crabs ( Limulus polyphemus ) [ 58 – 60 ]. These studies have generally provided limited evidence for IAV exchange from shorebirds to poultry, and some transfer between shorebirds and dabbling ducks [ 58 ].…”

“…One exception is a long-standing IAV surveillance effort in the U.S. that focuses on shorebirds, mainly ruddy turnstones (Arenaria interpres) , that migrate thru Delaware Bay, coinciding with mass numbers of breeding horse-shoe crabs ( Limulus polyphemus ) [ 58 – 60 ]. These studies have generally provided limited evidence for IAV exchange from shorebirds to poultry, and some transfer between shorebirds and dabbling ducks [ 58 ]. Other studies that focused on dissemination of IAVs in the Atlantic Flyway have investigated waterfowl, gulls, and murres inhabiting Newfoundland, a sampling location to the north of our study sites [ 51 , 52 , 57 , 61 ].…”