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A Review on the Prevalence of Poxvirus Disease in Free-Living and Captive Wild Birds

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A Review on the Prevalence of Poxvirus Disease in Free-Living and Captive Wild Birds Review A Review on the Prevalence of Poxvirus Disease in Free-Living and Captive Wild Birds Richard A. J. Williams 1,* , Daniel A. Truchado 2 and Laura Benitez 1 1 Departamento de Genética, Fisiología y Microbiología, Facultad de Biología, Universidad Complutense de Madrid C, José Antonio Nováis, 28040 Madrid, Spain; [email protected] 2 Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (CBGP, UPM-INIA), 28223 Madrid, Spain; [email protected] * Correspondence: [email protected]; Tel.: +34-913-944-963 Abstract: Avian pox is a widespread infection in birds caused by genus Avipoxvirus pathogens. It is a noteworthy, potentially lethal disease to wild and domestic hosts. It can produce two different conditions: cutaneous pox, and diphtheritic pox. Here, we carry out an exhaustive review of all cases of avian pox reported from wild birds to analyze the effect and distribution in different avian species. Avian poxvirus strains have been detected in at least 374 wild bird species, a 60% increase on a 1999 review on avian pox hosts. We also analyze epizootic cases and if this disease contributes to wild bird population declines. We frequently observe very high prevalence in wild birds in remote island groups, e.g., Hawaii, Galapagos, etc., representing a major risk for the conservation of their unique endemic avifauna. However, the difference in prevalence between islands and continents is not significant given the few available studies. Morbidity and mortality can also be very high in captive birds, due to high population densities. However, despite the importance of the disease, the current detection rate of new Avipoxvirus strains suggests that diversity is incomplete for this group, Citation: Williams, R.A.J.; Truchado, and more research is needed to clarify its real extent, particularly in wild birds. D.A.; Benitez, L. A Review on the Prevalence of Poxvirus Disease in Keywords: avian poxvirus; epidemiology; host range; prevalence; wild bird declines Free-Living and Captive Wild Birds. Microbiol. Res. 2021, 12, 403–418. https://doi.org/10.3390/ microbiolres12020028 1. Introduction Avian pox is an infectious disease of domestic and wild birds, caused by the transmis- Academic Editor: Takayuki Murata sion of viruses in the genus Avipoxvirus, family Poxviridae [1]. Poxviruses are large, linear, Received: 2 April 2021 double-stranded DNA viruses with a genome of 250–400 kb encoding 250–300 proteins. Accepted: 27 April 2021 They are amongst the largest animal viruses (~250 by 350 nm) and are oval or brick- Published: 30 April 2021 shaped [2]. Avian poxvirus (APV) has been detected in birds from all continents (including Antarctica [3]), as well as a number of remote islands. The virus can be transmitted directly Publisher’s Note: MDPI stays neutral between host individuals, environmentally, or mechanically by biting arthropods [4–6]. with regard to jurisdictional claims in The ICTV (International Committee on Taxonomy of Viruses) recognizes 12 species published maps and institutional affil- (and has proposed two more) in the genera Avipovirus [7], based on several criteria, iations. although the phylogenetic distance and natural host are the primary criteria used for the creation of new species and genera [8]. A molecular survey has identified 152 unique sequences [9], suggesting that APV species limits are far from resolved. Genetic analyses are dominated by studies of the 578 bp 4 b gene fragment (fpv167 locus), chosen because it Copyright: © 2021 by the authors. is relatively conservative between Avipoxvirus strains [10]. Most genetic lineages infect Licensee MDPI, Basel, Switzerland. multiple, taxonomically varied host species, suggesting that adaptation to specific host taxa This article is an open access article may be limited, at least for some strains [11,12]. It remains controversial whether strains distributed under the terms and are typically taxa specific or broad spectrum, and to what extent broad spectrum infection conditions of the Creative Commons is influenced by anthropogenic factors. Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/). Microbiol. Res. 2021, 12, 403–418. https://doi.org/10.3390/microbiolres12020028 https://www.mdpi.com/journal/microbiolres Microbiol. Res. 2021, 12,12 FOR PEER REVIEW 2 , 404 2.2. Host Host Range Range APVAPV was was reported reported to to have have been been detected detected in in278 278 species species of 23 of orders 23 orders in 1999 in 1999 [13]. [We13]. reportWe report in this in thisreview, review, that thatAPV APV has now has nowbeen beendetected detected in at inleast at least374 avian 374 avianspecies species from 23from orders 23 orders (Table (Table S1). APV S1). infects APV infects a broad a broadrange rangeof avian of avianhosts: hosts:from ostriches from ostriches to hum- to mingbirdshummingbirds and including and including domestic domestic birds, birds,raptors, raptors, parrots, parrots, waterbirds, waterbirds, seabirds, seabirds, etc. It has etc. beenIt has detected been detected in all major in all avian major orders, avian orders, except exceptfor Coraciiformes for Coraciiformes (kingfishers (kingfishers and allies), and probablyallies), probably because because this group this contains group contains relatively relatively few species few species(1.7% of (1.7% avian of species), avian species), which arewhich infrequently are infrequently in contact in contact with humans. with humans. Most APV Most detections APV detections (42%) (42%)have been have from been Passeriformes,from Passeriformes, the most the speciose most speciose bird order bird ( order61% of (61% species; of species; Figure Figure1). We1 carried). We carried out an exactout an binomial exact binomial test in testR version in R version 4.04 to 4.04 determine to determine whether whether the proportion the proportion of species of species in- fectedinfected with with APV APV in each in each order order (following (following Clements Clements et al. et [14]) al. [were14]) were higher higher or lower or lower than thethan expected the expected level of level 0.035% of 0.035% (Figure (Figure 2; Appendix2; Appendix A; TableA; S2). Table In S2).total, In APV total, was APV detected was fromdetected more from species more than species expected than expected (p < 0.005) (p < 0.005)in six inbird six orders bird orders (including (including “others”, “others”, an amalgamationan amalgamation of several of several minority minority orders; orders; explanation explanation Table Table S2) and S2) from and fromless species less species than expectedthan expected (p < 0.005) (p < 0.005) in four in bird four orders. bird orders. Bird orde Birdrs orders with more with moreAPV-positive APV-positive species species than expectedthan expected include include domestic domestic species species and larger and species larger (Galliformes, species (Galliformes, Anseriformes, Anseriformes, Psittaci- formes,Psittaciformes, Accipitriformes, Accipitriformes, Procellariformes Procellariformes and most and of most “others”—Struthioniformes, of “others”—Struthioniformes, Otidi- formes,Otidiformes, Ciconiiformes, Ciconiiformes, etc.). Bird etc.). orders Birdorders with less with APV-positive less APV-positive species species included included small andsmall cryptic and cryptic species species which are which potentially are potentially easier to easier overlook to overlook (Caprimulgiformes, (Caprimulgiformes, Passer- iformes,Passeriformes, Piciformes Piciformes and Coraciiformes) and Coraciiformes) and tend and to tend be tospeciose, be speciose, potentially potentially biasing biasing the results.the results. Figure 1. This word cloud (Wordart.com;(Wordart.com; accessed accessed 25 25 March March 2021) 2021) represents: represents: (A ()A the) the proportion proportion of of the the 10,721 10,721 avian avian species spe- cies in 41 avian [14] orders. For brevity, 24 orders constituting less than 1% of avian diversity are combined into “others”; in 41 avian [14] orders. For brevity, 24 orders constituting less than 1% of avian diversity are combined into “others”; (B) the (B) the number of species detected with APV in each order. Orders are color-coded to represent the percentage of avian number of species detected with APV in each order. Orders are color-coded to represent the percentage of avian species species found/cases of APV detected in each order, where blue and small represents <3%, green 3–7.5%, purple 7.5–11%, andfound/cases red and large of APV >11%. detected Although in each APV order, has wherebeen detected blue and in small more representsPasseriformes <3%, species green 3–7.5%,than non-Passeriformes purple 7.5–11%, species, and red moreand large APV >11%. are detected Although in non-Passeriformes APV has been detected than in morePasseriformes. Passeriformes Coraciiformes species than (light non-Passeriformes blue in (A), missing species, from more (B)) containsAPV are 1.7% detected of avian in non-Passeriformes species, though APV than has in Passeriformes. not yet been detected Coraciiformes in this order. (light blue in (A), missing from (B)) contains 1.7% of avian species, though APV has not yet been detected in this order. Microbiol.Microbiol. Res. 2021, 1212, FOR PEER REVIEW 3 , 405 Figure 2. Proportions (number (number of of APV APV species species in in partic particularular order/number order/number in in order. order. The The blue blue line line shows the expected expected level level
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