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.

Highlights

  • The movement of migrating birds, at both small scales and across broad latitudinal and longitudinal gradients, can serve to disseminate avian influenza A viruses (IAVs) and other pathogens overViruses 2020, 12, 1205; doi:10.3390/v12111205 www.mdpi.com/journal/virusesViruses 2020, 12, 1205 potentially long distances [1,2,3,4,5]

  • Subtypes of viruses recovered on the Atlantic Coast of northern Florida include H3N8 (n = 1) in January 2011, low pathogenicity (LP) H5N9 (n = 3) in March 2012, H6N1 (n = 9) in May

  • While IAV prevalence in ruddy turnstones in May at Delaware Bay (DE Bay) can be as high as 18% [13], the source(s) of IAVs in this unique system remains largely unknown

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Summary

Introduction

The movement of migrating birds, at both small scales and across broad latitudinal and longitudinal gradients, can serve to disseminate avian influenza A viruses (IAVs) and other pathogens overViruses 2020, 12, 1205; doi:10.3390/v12111205 www.mdpi.com/journal/virusesViruses 2020, 12, 1205 potentially long distances [1,2,3,4,5]. Wild birds in the orders Anseriformes (ducks and geese) and Charadriiformes (shorebirds, gulls, and terns) are known to have a role in the movement and maintenance of IAVs. While ducks and gulls have been shown to be critical to the long-term maintenance of IAV, shorebirds are thought to be important in the spread of viruses over long distances but on a shorter time scale [6]. Transmission of IAVs among ducks primarily occurs via a fecal-oral route [7], but less is known about transmission of IAVs among shorebirds Within both Anseriformes and Charadriiformes, the maintenance of IAVs is presumed to be continuous, though often at a low prevalence [8], such as is the case when these birds are on their wintering grounds. During May, large numbers of shorebirds (family Scolopacidae) and gulls

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