Families of Viruses that Affect Passeriformes: Comparison
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Please note this is a comparison between Version 2 by Sirius Huang and Version 1 by Richard Williams.

Interest in emerging viruses is growing because some can cause serious or lethal disease in humans and animals. The number of cloacal virome studies is also growing, however, these usually focus on poultry and other domestic birds, These studies reveal a wide variety of viruses, although the pathogenic significance of most newly discovered viruses is uncertain. Analysis of viruses detected in wild birds is complex and often biased towards waterfowl because of the obvious interest in avian influenza or other zoonotic viruses. Less is known about the viruses present in the order Passeriformes, which comprises approximately 60% of extant bird species. This review aims to compile the most significant contributions, from traditional and metagenomic studies, on the viruses that affect passerines. It highlights most passerine species have never been sampled. Some viruses, especially Flaviviridae, Orthomyxoviridae, Poxviridae and Togaviridae, and arguably others, are considered emerging because of increased incidence or avian mortality/morbidity, spread to new geographical areas or hosts and their zoonotic risk. However, many of these viruses have only recently been described in passerines using metagenomics and their role in the ecosystem is unknown.

  • biodiversity
  • DNA viruses
  • emergence
  • metagenomic studies
  • passeriformes
  • RNAviruses
  • spillover
  • zoonoses

1. Introduction

An emerging viral disease can be defined as a new occurrence of a disease because of: (a) the evolution or change of an existing virus or its spread to a new geographic area, species or ecological niche; (b) its rapidly increasing incidence, in terms of numbers of infected individuals or geographic range; or (c) a previously unrecognized disease or virus [1,2,3,4,5][1][2][3][4][5]. A viral disease of the past (i.e., one previously considered to be controlled) that re-appears with an increased prevalence in an area with susceptible host populations, expands its host range or appears in a new clinical form, is usually termed as re-emergent viral disease [4,6][4][6]. Many recent human emerging viral diseases have an animal origin, some with a significant impact on animal or public health, such as SARS-CoV-2, and two viruses that infect passerines: influenza A virus (AIV) and West Nile virus (WNV). The advent of modern, more powerful sequencing and bioinformatics technologies has increased the discovery of novel viruses in animals, with or without causing disease, that may be pathogenic, emergent, or zoonotic. Many of these novel and potentially emerging viruses are found in avian species that are present in virtually every ecosystem. Surprisingly, although passerines are the most abundant and diverse avian species worldwide, little is known about the novel and emerging viruses that they host and their possible role in the emergence of new viral diseases in animals and humans.
Several factors are related to the development of emerging viruses and diseases as they enable infectious agents to evolve into new ecological niches, to reach and adapt to new hosts, and to spread more easily among the new hosts: urbanization and destruction of natural habitats, allowing humans and animals to live in close proximity; international travels and trade; climate change and changing ecosystems; changes in populations of reservoir hosts or intermediate insect vectors [4,5][4][5]. All these inter-dependent factors imply that the study of new or emerging viruses must be approached from a multisectoral and multidisciplinary perspective, framed in the One Health approach supported by the WHO, WOAH and FAO [4,5][4][5] (Figure 1). The international trade of passerines, mainly ornamental breeds, has been also associated with the introduction of novel viruses in some countries, which pose a risk to native or endemic species if they can jump the species barriers, such as described with avipoxvirus in New Zealand [7]. There is also reasonable concern that more vulnerable individual species (of all taxa, including Passeriformes) may be at risk of extinction from viral pathogens. It is suggested that island endemic species are particularly vulnerable to pathogens, especially introduced pathogens to which they have no prior contact and no innate immunity [7]. Other authors have pointed out that all species with a small geographic range, low population size and low genetic diversity may be highly vulnerable to extinction, not just those island endemic species [8]. However, the researchers are not aware of any evidence that any species has ever become extinct due to a viral pathogen.
Microorganisms 11 02355 g001
Figure 1. The theoretical role of passerine birds in the circulation and potential spillover of viruses and other infectious agents to other passerines (blue semi-circular arrow around the bird in the center), domestic, peridomestic and other wild birds (blue bidirectional arrows) and their relation to potential zoonotic risk or threats to biodiversity (orange unidirectional arrows). The relation of passerines to theoretical consequences, such as zoonotic risk or threats to biodiversity, are depicted using orange unidirectional arrows. The One Health concept is represented by the light grey ring.
One of the most important factors that determines viral emergence is related to the adaptation of a given virus to new host species and/or the concomitant appearance of changes in the environment that offer new opportunities for the virus to thrive [9]. Some emerging viruses have a broad range of hosts. For example, RNA viruses such as West Nile virus (WNV) and Avian Influenza virus (AIV) can infect hundreds of different bird species including passerines. Others, such as herpesviruses or papillomavirus, are usually considered to be specific for one or a few related species [9,10][9][10]. Many species may act both as natural viral reservoirs and as amplifying hosts in bird-vector-bird cycles, for example, some togaviruses and flaviviruses. Occasionally these viruses are transmitted to incidental (dead-end) hosts including humans, equids, and other mammals. Birds can also act as a gene source of emerging viruses in cross-species transmission, for example, new influenza viruses may evolve through the reassortment of different gene segments [11].
The potential adaptation of an emerging virus to a new host depends on viral transmission routes (shedding of virus and infection in individuals) and the possibility of reaching this new host is facilitated by close and prolonged contact between individuals (such as breeding facilities). Viral transmission in birds may be horizontal (between individuals) or vertical (from females to offspring, congenitally or through embryonated eggs such as avian leukosis virus). Horizontal transmission is the most frequent and can occur by direct contact between animals (aerosols, fluids, feces, wounds or by predation or scavenging), by indirect contact through fomites or contaminated material (such as water, food, or troughs), and by vectors. Common vectors are blood-feeding arthropods such as mosquitos, midges, and ticks, in which the virus is propagated, and viruses transmitted mainly by this route are collectively called arboviruses (from Arthropod-Borne viruses). Vector-borne transmission is an indirect route of increasing importance in emerging viral diseases, some of which are important zoonoses, such as flaviviruses and togaviruses. It should be noted that viruses can be transmitted by more than one route.
Alternatively, viruses can enter the body via epithelial or the superficial mucosa of respiratory, gastrointestinal, and urogenital tracts. The most common routes of infection are ingestion of contaminated water or food (the fecal-oral route, for instance, picornaviruses) or inhalation of droplets expelled by an infected individual (respiratory route, for instance, herpesviruses and metapneumoviruses) or contaminated surfaces. Respiratory viruses can also be transmitted by contact with eye mucosa. In airborne transmission, viruses can spread over long distances through small respiratory aerosols that can remain suspended and travel in the air, such as influenza virus [12]. Viruses transmitted through ingestion usually are non-enveloped, resistant to low pH and to the acids in the digestive tract, and often produce diarrhea, causing large amounts of virus to be shed into the environment (where they can remain infectious for a long period of time) [9]. Diverse pathogens are probably transmitted between wild birds and domestic birds and poultry when feed and water are contaminated with feces in open aviaries and free-range farms. Describing the cloacal virome is essential for understanding the ecology of viruses circulating in the environment, identifying new virus-host relationships, and defining the risk of virus emergence [13]. However, data on the cloacal virome of wild or domestic passerines are still very scarce and, besides previous study in French Guiana and Spain [13], there are only a few other studies in China [14,15][14][15] and Australia/New Zealand [7,16,17][7][16][17]. Increased investigation of the virome and emerging viruses of passerines is vital for predicting future outbreaks and spillovers that can affect birds and other animals, humans and biodiversity [13,15][13][15].
Greater than two-thirds of viral taxa that infect humans are considered to be zoonotic: they are able to infect non-human vertebrates and may circulate in non-human reservoirs [18]. The alternative hosts for most zoonotic viruses are mammals (rodents, ungulates, other primates, carnivores, and bats). Birds are a much less important reservoir for zoonotic disease than mammals. Though less than 20% of zoonotic viruses share avian hosts [18], current data shows that birds are an important potential source for zoonotic viruses.
Passeriformes is the most diverse avian order. These are songbirds and perching birds with well-known species including sparrows, starlings, thrushes, magpies, crows, swallows, and finches. There are around 10,700 bird species, placed in 41 orders and 248 families, of which nearly 6400 species (59.6%) and 140 families (56.5%) are Passeriformes [19], making it by far the most speciose avian family. In addition, many passerine species are also extremely abundant. One recent estimate of the abundance of 92% of bird species determined that there are approximately 50 billion individual birds (albeit with high levels of uncertainty), of which 28 billion (56%) are Passeriformes [20]. This begs the question of whether the diversity of viruses circulating in Passeriformes is approximately equal to their share of avian diversity and abundance, and whether they could pose a significant risk to human and animal health and environmental balance.
Passerines include wild, urban, rural, and pet birds. Many passerine species are extremely abundant in the wild, but many populations of passerines are synanthropic species that live in close proximity to anthropogenic environments, which boosts the risk of the circulation of viral diseases between humans [21] poultry, and passerines (Figure 1). Pet passerines are usually bred for ornamental use, kept in captivity at home or in different types of aviaries (e.g., breeding facilities) that may have access to outdoors increasing the risk of contact with wild birds [22]. Migratory passerines can spread a wide variety of viruses over long distances, potentially being capable of infecting resident wild passerines (such as house sparrows, Passer domesticus), and these latter possibly contaminating pet birds living in open aviaries or poultry in farms [22]. For example, it has been suggested that small passerines could serve as bridge hosts for low-pathogenic avian influenza virus (LPAI) from infectious waterfowl to commercial turkey farms [23]. It is possible that the contact zone between agriculture and wildlife provides an interface where viruses could potentially circulate between wild and domestic birds [23] but probably vice versa as well. Passerines could play a larger role than previously thought in this interaction, a hypothesis that needs to be further studied.

2. Families of Viruses Affecting Passeriformes

The most important families of viruses affecting passerine birds are shown in Figure 2. Data on the bird species and families these viruses affect is summarized in Table 1, Tables S1 and S2 (can be downloaded at: https://www.mdpi.com/article/10.3390/microorganisms11092355/s1, Table S1: List of bird species; Table S2: List of avian families). Species recognized by the International Committee on Taxonomy of Viruses (ICTV) are italicized.
Figure 2. Viral transmission routes in passeriform birds. DNA viruses are shown in blue and RNA viruses in green. Avian Influenza virus (AIV), Avian leukosis virus (ALV), APMV (Avian paramyxovirus), APV (Avian papillomavirus), BCRV (Buggy Creek virus), BFDV (Circovirus), CaCV (Circovirus), CNPV (Canary poxvirus), CoHV-1 (Columbid herpesvirus-1), CoV (coronavirus), HEV (hepevirus), CRESS-DNA viruses (circular-rep encoded single stranded DNA), CV (calicivirus), EEEV (Equine eastern encephalitis virus), Estrildidae adenovirus (EsAdV), FcPV (Fringilla coelebs papillomavirus), FGPV (Picornavirus), FWPV (Fowlpox virus), GFAdV-1 (Gouldian finch adenovirus-1), GTAdV-1 (great tit adenovirus-1), HPAI (Highly pathogenic Avian Influenza), HJV (Highland J virus), MAYV (Mayaro virus), PaHV-1 (Passerid herpesvirus-1), PaPV (Passerid parvovirus), PasAstV (Passerid astrovirus), Passerid adenovirus-1 (PaAdV-1), PsHV-1 (Psittacid herpesvirus-1), RRV (Ross River virus), RVA (rotavirus), ScPV1 (Serinus canaria papillomavirus), SINV (Sindbis virus), SLEV (Saint Louis Encephalitis virus), USUV (Usutu virus), and WNV (West Nile virus).
Table 1. Virus names, abbreviations and genus/species designations are listed according to the taxonomy and nomenclature approved by the International Committee on Taxonomy of Viruses (ICTV) [294][24]. All ICTV accepted viral taxa are in italics.
Viral Family Genus Viral Taxa Abbreviations Nomenclature Bird Family Clinical Signs Mortality Rate References
dsDNA VIRUSES  
Herpesviridae Iltovirus Gallid herpesvirus 1 GaHV-1 Iltovirus gallidalpha1 Turdidae, Estrildidae, Sturnidae Subclinical infection/

Respiratory signs		 High [7,26,34,7][25]35,[26]37][[27][28]
Psittacid herpesvirus 1 PsHV-1 Iltovirus psittacidalpha1 Sturnidae
passerid herpesvirus 1   not recognized Fringillidae
Mardivirus Columbid herpesvirus 1 CoHV-1 Mardivirus columbidalpha1 Corvidae, Turdidae Subclinical infection Probably not [40][29]
Poxviridae Avipoxvirus Fowlpox virus (Lineage A1) FWPV same Fringillidae, Passeridae Cutaneous lesions/Upper respiratory and digestive tract lesions High [42,43,53,54][30][44,3145,46,][3247,][3348,][3449,]35][36][3750,][3851,[][52,39][40][41][42]
Pigeonpox virus (Lineage A2) PGPV same Fringillidae High/Medium
Accipitriformespox virus (Lineage A7)   same Lanidae High/Medium
Canarypox virus (Lineage B1) CNPV same Fringillidae, Paridae, Corvidae (and 11 other families) High/Medium
Starlingpox virus (Lineage B2)   same Sturnidae, Passeridae High/Medium
Lineage B3 poxvirus   not recognized Corvidae (and eight other mostly Passeriformes families) High
Adenoviridae Atadenovirus European robin adenovirus   not recognized Meliphagidae, Fringillidae, Ploeceidae, Estrildidae, Turdidae, Ptilonorhynchidae, Sturnidae, Zosteropidae, Maluridae, Petroicidae Subclinical infection/

Not known		 Probably not [57,58][43][44]
European greenfinch adenovirus   not recognized
Eurasian siskin adenovirus   not recognized
Eurasian bullfinch adenovirus   not recognized
common chaffinch adenovirus   not recognized
passerine adenovirus 1   not recognized
white plumed honeyeater adenovirus 1, -2   not recognized
vitelline masked weaver adenovirus strains 37869 and 38132   not recognized
Aviadenovirus great tit adenovirus strain 47292   not recognized Fringillidae, Estrildidae, Paridae, Ploceidae, Sylvidae, Falcunculidae, Petroicidae Subclinical infection/

Not known		 Probably not  
european greenfinch adenovirus   not recognized
goldfinch adenovirus   not recognized
vitelline masked weaver adenovirus strain 39658   not recognized
Siadenovirus double-barred finch adenovirus   not recognized Estrildidae, Paridae, Sylvidae, Thraupidae, Meliphagidae, Pardalotidae, Rhipiduridae, Sturnidae Subclinical infection/

Probable renal lesions		 Probably not [56,60][45][46]
eurasian blackcap adenovirus   not recognized
gouldian finch adenovirus 1 GFAdV-1 not recognized
great tit adenovirus strain 47292 GTAdV-1 Great tit siadenovirus A
zebra finch adenovirus strain 47535   not recognized        
Papillomaviridae Etapapillomavirus Fringilla coelebs Papillomavirus 1 FcPV1 Etapapillomavirus 1 Fringillidae Cutaneous lesions Low [66,4767,][4869,][4970,]71,72][[50][51][52]
Serinus canaria papillomavirus 1 ScPV1 not recognized Fringillidae Not known Not known [68][53]
ssDNA VIRUSES  
Circoviridae Circovirus Beak and feather disease virus BFDV Circovirus parrot Artamidae, Corvidae, Estrildidae, Fringillidae, Petoicidae, Sturnidae, Thamnophilidae Feather lesions Probably not [76,77,78][54][55][56]
Circovirus canary CaCV same Feather diseases and immunosupression/

Subclinical infection		 Yes/Not known [25,79,80,81,82][57][58][59][60][61]
Circovirus finch FiCV same
Circovirus raven RaCV same
Circovirus starling StCV same
Circovirus zebrafinch ZfiCV same
Cyclovirus Robinz virus RP_736 RobinzV736 Cyclovirus cervienka Petroicidae Not known Not known [17]
Robinz virus RP_1170 RobinzV1170 Cyclovirus liepsnele
Robinz virus RP_493 RobinzV493 Cyclovirus pettirosso
Robinz virus RP_620 RobinzV620 Cyclovirus prihor
Robinz virus RP_526 RobinzV526 Cyclovirus punarinta
Robinz virus RP_584 RobinzV584 Cyclovirus rudzik
Robinz virus RP_259 RobinzV259 Cyclovirus totoi
Probably new genus Gyrovirus 11   not recognized Thamnophilidae Not known Not known [89][62]
Genomoviridae Gemycirculavirus new species   not recognized Petroicidae, Aegithalidae, Corvidae, Emberizidae, Fringillidae, Muscicapidae, Paridae, Sylviidae, Turdidae, Zosteropidae Not known Not known [88][63]
Chickadee associated gemycircularvirus 1   Gemycircularvirus chickad1 Paridae [85][64]
Finch associated genomovirus 5   Gemycircularvirus haeme1 Fringillidae [86][65]
Finch associated genomovirus 6   Gemycircularvirus haeme2 [86][65]
Gemykibivirus Blackbird associated gemykibivirus 1   Gemykibivirus blabi1 Turdidae [87][66]
Black robin associated gemykibivirus 1   Gemykibivirus blaro1 Petroicidae
Finch associated genomovirus 3   Gemykibivirus haeme1 Fringillidae [86][65]
Finch associated genomovirus 2   Gemykibivirus haeme3
Finch associated genomovirus 4   Gemykibivirus haeme4
Finch associated genomovirus 1   Gemykibivirus haeme5
Gemykroznavirus Finch associated genomovirus 8   Gemykronzavirus haeme1 Fringillidae
Gemygorvirus Starling associated gemygorvirus 1   Gemygorvirus stara1 Sturnidae [87][66]
Parvoviridae Aveparvovirus Aveparvovirus passeriform1 PfPV same Thraupidae Not known Not known [95][67]
ssRNA VIRUSES  
Orthomyxoviridae Alphainfluenzavirus 1 Highly Pathogenic Avian Influenza H5N1 FLUAV/(H5N1) Alphainfluenzavirus influenzae Passeridae, Turdidae, Ploceidae, Corvidae, Hirundidae, Icteridae (and many other families) Mild/Severe disease High [101,102,103,104,105,106,107,108,110,116][68][69][70][71][72][73][74][75][76][77]
Paramyxoviridae Orthoavulavirus Avian paramyxovirus 1 (NDV, Newcastle Disease virus) APMV-1 Orthoavulavirus javaense Passeridae, Motacillidae, Passarellidae Not known/Subclinical disease High/Not known [113,123,124,126,127][78][79][80][81][82]
Metaavulavirus Avian paramyxovirus 2 APMV-2 Metaavulavirus yucaipaense Corvidae, Motacillidae, Troglodytidae, Muscicapidae, Emberizidae, Estrildidae Mild/Severe disease [128,83129,130,][84131,][85132,]133,134][[86][87][88][89]
Paraavulavirus Avian paramyxovirus 3 APMV-3 Paraavulavirus wisconsinense [135,136][90][91]
Paraavulavirus Avian paramyxovirus 4 APMV-4 Paraavulavirus hongkongense [138][92]
Pneumoviridae Metapneumovirus Avian metapneumovirus AMPV Metapneumovirus avis Passeridae, Sturnidae Not known Not known [141,142][93][94]
Bornaviridae Orthobornavirus Estrildid finch bornavirus 1 EsBV-1 Orthobornavirus estrildidae Estrildidae, Corvidae, Fringillidae Not known Not known [146,147,148,[96][97149][95]][98]
Canary bornavirus 1 CnBV-1 Orthobornavirus serini
Canary bornavirus 2 CnBV-2
Canary bornavirus 3 CnBV-3
Flaviviridae Orthoflavivirus 1 Japanese encephalitis virus JEV Orthoflavivirus japonicum Passeridae, Corvidae, Fringillidae, Turdidae (and >23 more families) Not known High [183][99]
Saint Louis encephalitis virus SLEV Orthoflavivirus louisense [191,192,193,194][100][101][102][103]
Murray Valley Encephalitis virus MVEV Orthoflavivirus murrayense [186][104]
Usutu virus USUV Orthoflavivirus usutuense Severe disease [174,175,176][105][106][107]
West Nile virus WNV Orthoflavivirus nilense Mild/Severe disease [158,159,160,161,162,169][108][109][110][111][112][113]
Togaviridae Alphavirus 1 Eastern equine encephalitis virus EEEV same Turdidae, Hirundidae, Icteridae, Petroicidae, Estrildidae, Monarchidae Neurological disease Yes [206,207,208][114][115][116]
Highlands J virus HJV same Mild disease [210][117]
Sindbis virus SINV same Severe disease [215,[118216]][119]
Ross River virus RRV same Not known [219,220][120][121]
Mayaro virus MAYV same [225,226,227,228][122][123][124][125]
Buggy Creek virus BUCGV Fort Morgan virus Neurological disease [230,231,232][126][127][128]
  Deltacoronavirus 2 Bulbul coronavirus HKU11 BulCV_HKU11 same Turdidae, Estrildidae, Pycnonotidae, Passeridae, Zosteropidae, Fringillidae, Emeberizidae Severe disease Probably high [239,240,241][129][130][131]
Munia coronavirus HKU13 MunCV_HKU13 same
Thrush coronavirus   not recognized
White-eye coronavirus HKU16 WECoV_HKU16 same
Coronavirus HKU15 PoCoV_HKU15 same
Picornaviridae Oscivirus Oscivirus A1 and A2 (turdivirus 2 and 3) OsV-A1/OsV-A2 Oscivirus A Turdidae, Muscicapidae Severe disease Not known [247,248][132][133]
Passerivirus Passerivirus A and B PasV-A/PasV-B same Turdidae, Estrildidae High
Poecivirus Poecivirus A1 PoeV-A Poecivirus A Paridae Yes [251,252][134][135]
Probably new genus French Guiana Picornavirus FGPV not recognized Thamnophilidae Not known Not known [13]
Astroviridae Avastovirus novel avastrovirus clades 4 and 5   not recognized Fringillidae, Monarchidae Parulidae, Passeridae Subclinical infectionMild disease Not known [258,259,260][136][137][138]
Caliciviridae Probably new genera new calicivirus   not recognized Prunellidae, Turdidae, Emberizidae, Fringillidae, Muscicapidae, Petroicidae Subclinical infection Not known [7,15,275,276][7][15][139][140]
Hepeviridae Probably new genera new hepe-like viruses   not recognized Thamnophilidae, Turdidae, Zosteropidae Not known Not known [7,13,15][7][13][15]
dsRNA VIRUSES  
Reoviridae Orthoreovirus 2 new orthoreovirus   not recognized Emberizidae, Turdidae, Fringillidae Not known High mortality [283,284][141][142]
RNA REVERSE TRANSCRIBING VIRUS  
Retroviridae Alpharetrovirus Avian leukosis virus ALV same Emberizidae, Paridae, Corvidae, Muscicapidae, Thraupidae, Phylloscopidae Subclinical infection Possibly [291,292,293][143][144][145]
1: Zoonotic risk; 2: Doubtful zoonotic risk.

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