Coronaviruses in wild birds – A potential and suitable vector for global distribution

Abstract The recurrent appearance of novel coronaviruses (CoVs) and the mortality and morbidity caused by their outbreaks aroused a widespread response among the global science community. Wild birds' high biodiversity, perching and migratory activity, ability to travel long distances and possession of a special adaptive immune system may make them alarming sources of zoonotic CoV‐spreading vectors. This review gathers the available evidence on the global spread of CoVs in wild birds to date. The major wild birds associated with different types of CoVs are Anseriformes, Charadriiformes, Columbiformes, Pelecaniformes, Galliformes, Passeriformes, Psittaciformes, Accipitriformes, Ciconiiformes, Gruiformes and so on. However, the main type of CoVs found in wild birds is gammacoronavirus, followed by deltacoronavirus. Consequently, it is imperative to enable thorough research and continuous monitoring to fill the study gap in terms of understanding their role as zoonotic vectors and the frequent appearance of novel CoVs.

origin was connected to a wholesale seafood market in Wuhan, China (Zhu et al., 2020). According to the "Coronavirus disease 2019 (COVID-19) Situation Report-101" by WHO, published on 30 April 2020, SARS-CoV-2 has taken 217,769 (7.05%) lives out of 3,090,445 confirmed cases, and the death toll is still rising.
Birds are natural pools for supplying viral genes during the development of new species and viruses for interspecies transmission.
These warm-blooded vertebrates show high species biodiversity, perching and migratory conduct, ability to fly long distances and possession of a remarkably versatile immune system, which are ideal qualities for asymptomatic shedding, dispersal and blending of various viruses for the development of novel mutant, recombinant or reassortant RNA viruses. The expanded incursion of people into wildlife habitats and congestion of various natural species in wet markets and ranches have likewise encouraged interspecies transmission among various animals (Chan et al., 2013). Throughout the years wild birds have been under epidemiological observation because these act as a natural repository of many growing zoonotic pathogens and, therefore, significantly affect public health (Miłek & Blicharz-Domańska, 2018). They are pervasive and exceptionally versatile potential hosts equipped for moving viruses past topographical and political boundaries and have been implicated in the spread of profoundly pathogenic H5Nx avian influenza viruses, tickborne encephalitis virus, West Nile virus, Newcastle disease virus (NDV) and influenza A virus (IAV) (Hepojoki et al., 2017).

Regular interspecies spillover of CoVs occurs to new hosts, with
SARS-CoV and MERS-CoV being the most noteworthy examples of spillover into humans. Bovine CoV, canine respiratory CoV, dromedary camel CoV and even human CoV OC43 all probably come from the same common ancestor, demonstrating substantial host versatility (Lu et al., 2017;Nathalie et al., 2016;Vijgen et al., 2005).

SARS-CoV possibly originated in bats, whereas Porcine Diarrhea
CoV may, interestingly, have emerged in birds (Lau et al., 2005;Ma et al., 2015). The 2003 SARS-CoV outbreak deeply influenced the global medical, economic and social spheres, revitalizing interest in CoV research. One crucial discovery was the recognition of bats as the natural repository for viruses and of civet and other mammals as SARS-CoV intermediate amplifying hosts. The subsequent advent of MERS-CoV marked a new era in CoV research history (Lau et al., 2005). Such findings reshaped the "hunting" approach for novel CoVs and reshaped the classification of CoVs on the basis of theirs updated phylogeny and the crucial function of bats in the inter-and intra-species transmission of CoVs (Chan et al., 2013).
In this review, we present an updated scenario on the distribution of CoVs in wild birds worldwide to emphasize their role as a natural pool and possible potential zoonotic vector in spreading and evolving novel CoVs.

| CORONAVIRUS E S
CoVs consist of a family of the order Nidovirales (Coronaviridae family). The CoV genome is among the largest genomes of viral RNA (25-32 kb) (Flint et al., 2015). CoVs are classified into four separate genera, based on phylogenetic analysis: alpha-, beta-, gamma-, and delta-CoV. Mammals bear the alpha-and beta-CoVs, whereas the gamma-and delta-CoVs primarily infect birds, with few deviations. This can be further subclassified into lineages A, B, C and D within beta-CoV (De-Groot et al., 2012;King et al., 2011). In 2018, these four lineages were reclassified as beta-CoV subgenera and renamed embecovirus (former lineage A), sarbecovirus (former lineage B), merbecovirus (former lineage C) and nobecovirus (former lineage D).
This also contained a fifth subgenus, hibecovirus (ICTV 2019;Wong et al., 2019). The major factors contributing to the high genetic diversity of CoVs are the large genomes, the RNA-dependent polymerase infidelity, and the high frequency of homologous RNA recombination (Denison et al., 2011;Jackwood et al., 2012;Woo et al., 2009).

| China and Hong Kong
A study conducted by Chu et al. (2011) in China showed that 12% of screened, apparently healthy, wild aquatic birds (Anseriformes, Pelecaniformes and Ciconiiformes) were found with F I G U R E 1 Wild birds across the world from different ecology, climate and geography are carrying coronaviruses (based on the Google world map) gamma-CoV and delta-CoV. Gamma-CoVs were present mainly in birds of Anseriformes, whereas delta-CoV was identified in birds of Ciconiiformes, Pelecaniformes and Anseriformes in this analysis.
The authors found that gamma-CoV interspecies transmissions between duck species were frequent. In contrast, delta-CoV may have host specificities that are more stringent. The avian viral and host sequences of mitochondrial DNA also suggest that some CoV may have coevolved with birds of the same order, but not all. A total of 658 samples were tested and gathered in Hong Kong. Ninety-nine (15%) of those samples were positive for CoV reverse transcription (RT)-PCR. Both CoVs found in this study were listed as gamma-CoV and delta-CoV in phylogenetic terms (Chu et al., 2011). In recent years, In recent years, the understanding of viral diversity has been increased significantly due to the rapid discovery of novel viruses utilizing next-generation sequencing technologies particularity DNA-Seq and RNA-Seq (Chen et al., 2013). Using RNA-Seq, Chen et al. (2013) described a novel duck CoV within the gamma-CoV family, distinct from chicken IBV, as shown by sequences in the viral 1b gene from three regions. A survey of domestic Chinese fowls using RT-PCR targeted to the viral nucleocapsid gene found a total of 102 positive CoVs. Besides, the findings presented novel data supporting the notion that certain host-specific CoVs other than IBVs circulate in ducks, geese and pigeons and suggested that the novel duck-specific CoV found in this study by RNA-Seq is genetically closer to certain CoVs that circulate in wild waterfowl (Chen et al., 2013).

| Cambodia
Meanwhile, in Cambodia, Chu et al. (2011) collected cloacal swabs (263) from pond herons, lesser whistling ducks and ruddy-breasted crakes. CoV-positive reactions were observed in pond herons at 13.0% (16/123) and lesser whistling ducks at 3.0% (1/33). Kim and Oem (2014) analysed the oropharyngeal swabs of 32 species of wild birds. The 14 avian CoVs found belonged to the gamma-CoV and shared homology with some previously described strains in wild waterfowl but not with IBVs, showing a high-nucleotide sequence identity. Of the 1,473 samples analysed, 14 (0.95%) were positive. The authors found CoVs in two species of waterfowl: 1 of 96 northern pintails (Anas acuta; 1%) and 13 of 361 Indian spot-billed ducks (Anas poecilorhyncha; 3.6%). The partial viral RdRp sequences were determined from 14 CoVs and compared with those from 32 other CoVs of interest. All detected CoVs were phylogenetically categorized as gamma-CoV along with 2 Korean IBV strains (SNU8067 and KM91), and the 14 Korean CoVs' RdRp segment showed more than 93% homology sequence (Kim & Oem, 2014).

| Indonesia
In Bogor, West Java, Indonesia, an IB-like avian CoV was isolated from healthy Eclectus parrots (Eclectus roratus) belonging to a bird breeder (Suryaman et al., 2019). The parrot Eclectus is a native bird to Indonesia and Northern Australia and is mostly kept as a pet. The similarity between captive bird-isolated viruses and those in domesticated poultry was troubling because there was an indication that a reverse spillover effect had already occurred from poultry farms into the ecosystem. Wild birds and other non-Galliform Aves may harbour IBV or IB-like CoV without displaying any symptoms and reflect the wide variety of CoV in the host.

| England
Wildfowl (Anseriformes) and waders (Charadriiformes) were recorded in England for carrying CoVs (Hughes et al., 2009). CoV RNA was observed in 7 faecal sample pools, providing an approximate prevalence of 1.6% at individual bird level. Of those pools with positive CoV outcomes, four were obtained from ducks.
Another pool had samples of whooper swans (Cygnus cygnus), one sample of red knots (Calidris canutus) and one sample of Eurasian oyster catchers (Haematopus ostralegus). PCR-positive pools were in the estuarine, salt marsh or standing water environments from birds sampled. All the birds were relatively well. Although samples from wild bird populations comprising 46 species from various and F I G U R E 2 Distribution of major wild birds (order) detected with coronaviruses in studied countries worldwide TA B L E 1 A brief overview of the studies conducted on the prevalence and distribution of Coronaviruses in wild birds all over the world

| Norway
A Norwegian study by Jonassen et al. (2005) recorded that the prev-

| Sweden
CoV infections in mallard ducks (Anas platyrhynchos) were also recorded in Sweden, with one of the studies showing a prevalence of CoV infections with the seasonal variation of 6.9%. The prevalence of CoVs among wild waterbirds in Sweden was reported by Wille et al. (2016) to be only 18.7%, which is higher than many other wild bird surveys. In this study, a total of 764 birds from 11 Anseriform species (ducks, geese, swans) and 11 species of Charadriiformes (gulls, terns, shorebirds) were sampled. However, the organisms, groups and orders were poorly described. Diving ducks were found with the highest prevalence (39%). Although the sample size was small (37) Canuti et al. (2019) reported that a novel GuCoV (B29)

| Beringia
A study by Muradrasoli et al. (2010) carried out in the Beringia (comprising areas of Alaska and Siberia) indicated gamma-CoVs RNA in 6.4% of the birds tested (Anseriformes, Pelecaniformes and Charadriiformes). Some of the sequences found in the Chinese sample were intriguingly similar to those found in the Beringia region.
Samples from 26 bird species were tested with RT-PCR for the CoVs polymerase (RdRp) gene, and 64 of the 1,002 faecal and cloacal samples were positive (6.4%). Positives of 18 species were identified.
The researchers divided the species into six groups, which represented both their taxonomy and ecology. Such groups were geese (5 species), waders (9 species), gulls (6 species), ducks (1 species), auks (2 species) and seabirds (3 species). All 18 CoV-positive bird species contained gamma-CoV, and there was a major variation in PCR positivity among bird groups. Wader species were more often recorded as CoV positive (17.1%), followed by ducks (11.5%), geese (8.2%), gulls (3.1%) and seabirds (1.5%), although auks had the lowest prevalence (0.8%). By comparison, none of the 101 tufted puffins studied were CoV positive. CoVs in Beringia are common among wild birds, and their regional distribution and frequency are higher than previously thought. Chamings et al.'s (2018) (Lima et al., 2015). This lake has a rich wildlife ecosystem with a fairly large number of endemic, uncommon and endangered species (Ferry et al., 2009;Guerrini et al., 2014). Given the results in the samples examined here on the identification of avian CoVs, it may be concluded that these viruses are common among birds found in this area. The identification of gamma-CoV sequences in this area of study, and geographically distinct regions such as Russia, Alaska and Cambodia, do indeed suggest that CoVs are common among birds associated with water ecosystems, raising concerns about potential consequences for wildlife and poultry development (Lima et al., 2015).  (Barbosa et al., 2019). Although it is difficult to foresee, many migratory species may have past interaction with migratory birds from Western/Central Siberia, the Balkans, the Black Sea and Central Asia using East African flyways to enter wintering areas to rest along with the river systems that cross the Arab Peninsula and the Nile (Lima et al., 2015). The direct transfer of an infectious agent is rarely reported from wild birds to humans. Potential causes and strategies for the spread of infectious agents from birds to humans require further exploration (Gilbert et al., 2006;Olsen et al., 2006;Reed et al., 2003;Tsiodras et al., 2008;Verhagen et al., 2015).

| CON CLUS ION
Globally, CoVs are widespread in several species of wild birds. The data on the prevalence of CoVs in wild birds across the world are scarce. Wild bird species of certain countries or locations are linked by one or more bird migration routes, which may encourage the spreading of native CoVs to the global wild bird and other animal populations. Moreover, interspecies transmission poses a great risk for spreading, mutation and the emergence of new strains of the viruses.
To recognize their contribution to evolving novel viruses and zoonotic diseases, region-specific and outcome-based studies need to be conducted immediately with continuous surveillance of wild birds.

CO N FLI C T O F I NTE R E S T
The authors announce that there is no conflict of interest.

PE E R R E V I E W
The peer review history for this article is available at https://publo ns.com/publo n/10.1002/vms3.360.