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viruses Article Influenza A Viruses in Whistling Ducks (Subfamily Dendrocygninae) Deborah L. Carter 1, Paul Link 2, Gene Tan 3,4, David E. Stallknecht 1 and Rebecca L. Poulson 1,* 1 Southeastern Cooperative Wildlife Disease Study, Department of Population Health, College of Veterinary Medicine, The University of Georgia, 589 D. W. Brooks Dr., Athens, GA 30602, USA; [email protected] (D.L.C.); [email protected] (D.E.S.) 2 Louisiana Department of Wildlife and Fisheries, 2000 Quail Drive, Room 436, Baton Rouge, LA 70808, USA; [email protected] 3 J. Craig Venter Institute, 4120 Capricorn Lane, La Jolla, CA 92037, USA; [email protected] 4 Division of Infectious Diseases, Department of Medicine, University of California, La Jolla, San Diego, CA 92037, USA * Correspondence: [email protected] Abstract: As compared to other Anseriformes, data related to influenza A virus (IAV) detection and isolation, and IAV antibody detection in whistling ducks (Dendrocygna spp. and Thalassornis leuconotus; subfamily Dendrocygninae) are limited. To better evaluate the potential role of whistling ducks in the epidemiology of IAV, we (1) conducted surveillance for IAV from black-bellied whistling ducks (BBWD, Dendrocygna autumnalis) sampled in coastal Louisiana, USA, during February 2018 and 2019, and (2) reviewed the published literature and Influenza Resource Database (IRD) that reported results of IAV surveillance of whistling ducks. In the prospective study, from 166 BBWD sampled, one H10N7 IAV was isolated (0.6% prevalence), and overall blocking enzyme-linked immunosorbent assay (bELISA) antibody seroprevalence was 10%. The literature review included publications and data in the IRD from 1984 to 2020 that reported results from nearly 5000 collected samples. For any given collection, the IAV isolation rate never exceeded 5.5%, and seroprevalence estimates Citation: Carter, D.L.; Link, P.; Tan, ranged from 0 to 42%. Results from our prospective study in Louisiana are consistent with this G.; Stallknecht, D.E.; Poulson, R.L. historic literature; however, although all data consistently demonstrated a low prevalence of infection, Influenza A Viruses in Whistling Ducks (Subfamily Dendrocygninae). the potential role of this species in the epidemiology of IAV should not be totally discounted. In sum, Viruses 2021, 13, 192. https://doi.org/ whistling ducks can be infected with IAV, they represent important species on many areas where 10.3390/v13020192 waterfowl winter, and their distribution across the globe appears to be changing. Academic Editor: Ignacio Nacho Mena Keywords: avian influenza; Dendrocygninae; host; IAV; prevalence; surveillance; whistling ducks Received: 31 December 2020 Accepted: 27 January 2021 Published: 28 January 2021 1. Introduction Publisher’s Note: MDPI stays neutral Wild waterfowl in Order Anseriformes are important natural reservoirs for influenza with regard to jurisdictional claims in A virus (IAV), but there have been limited reports of IAV in species of whistling ducks published maps and institutional affil- (WD; Family Anatidae, Subfamily Dendrocygninae). One of the eight currently recognized iations. species of WD, the black-bellied whistling duck (BBWD; Dendrocygna autumnalis) is com- mon in the Americas. BBWD breed throughout Louisiana, Texas, Mexico, and Central and South-central America, and form large flocks when not breeding, often in association with fulvous whistling ducks (FUWD; Dendrocygna bicolor)[1]. BBWD are largely residential Copyright: © 2021 by the authors. apart from local movement, and tropical populations of BBWD are migratory with move- Licensee MDPI, Basel, Switzerland. ment in the winter months [1]. The distribution of the species is expanding, and BBWD This article is an open access article are now abundant along the southeastern coast of the United States [2]. Nocturnal feeders, distributed under the terms and BBWD forage on seeds, aquatic invertebrates, and vegetation in shallow freshwater [3]. conditions of the Creative Commons In addition to the BBWD and FUWD, six other WD species are recognized worldwide in Attribution (CC BY) license (https:// genus Dendrocygna, including Dendrocygna arborea (West Indian WD); Dendrocygna arcuata creativecommons.org/licenses/by/ (wandering WD), Dendrocygna eytoni (plumed WD), Dendrocygna guttata (spotted WD), 4.0/). Viruses 2021, 13, 192. https://doi.org/10.3390/v13020192 https://www.mdpi.com/journal/viruses Viruses 2021, 13, x FOR PEER REVIEW 2 of 10 Viruses 2021, 13, 192 In addition to the BBWD and FUWD, six other WD species are recognized worldwide2 of 10 in genus Dendrocygna, including Dendrocygna arborea (West Indian WD); Dendrocygna arcu- ata (wandering WD), Dendrocygna eytoni (plumed WD), Dendrocygna guttata (spotted WD), DendrocygnaDendrocygna javanicajavanica (lesser(lesser WD;WD; LEWD),LEWD), andand DendrocygnaDendrocygna viduataviduata (white-faced(white-faced WD;WD; WFWD);WFWD); the white-backed duck duck (Thalassornis (Thalassornis leuconatus leuconatus) )is isalso also classified classified in inthe the Dendrocyg- Dendro- cygninaeninae subfamily. subfamily. Broadly, Broadly, WD WD primarily primarily exhi exhibitbit only only localized movements withinwithin theirtheir breedingbreeding ranges, ranges, with with some some exceptions. exceptions. Small Sma populationsll populations of LEWD of LEWD in Asia in haveAsia been have noted been tonoted leave to their leave northernmost their northernmost breeding breeding areas in area thes winterin the winter [4], and [4], the and globally the globally widespread wide- FUWDspread areFUWD migratory are migratory only inthe only most in the northern most no portionsrthern portions of their Mexican of their Mexican range [5]. range [5]. ThoughThough infrequentlyinfrequently sampledsampled asas comparedcompared toto somesome otherother speciesspecies inin OrderOrder Anser-Anser- iformes,iformes, exposureexposure toto andand infectioninfection ofof IAVIAV hashas beenbeen detecteddetected inin residentresident andand migratingmigrating Dendrocygninae,Dendrocygninae, mostly mostly outside outside of of the the United United States. States. ToTo better better understand understand the the role role of of WD WD inin thethe ecologyecology ofof IAV,IAV, we we (1) (1) conducted conducted IAV IAV surveillance surveillance of of wintering wintering BBWD BBWD along along the the GulfGulf coastcoast ofof thethe UnitedUnited StatesStates overover twotwo years,years, andand (2)(2) reviewedreviewed publishedpublished literatureliterature and and thethe InfluenzaInfluenza Resource Resource Database Database (IRD) (IRD) [ [6]6] forfor resultsresults fromfrom worldwideworldwide surveillancesurveillance forfor IAVIAV inin thisthis avianavian subfamily.subfamily. 2.2. MaterialsMaterials andand MethodsMethods 2.1.2.1. VirusVirus IsolationIsolation andand AntibodyAntibody DetectionDetection CloacalCloacal andand oropharyngealoropharyngeal (COP)(COP) swabsswabs andand serumserum werewere opportunisticallyopportunistically collected collected fromfrom live-capturedlive-captured BBWDBBWD inin thethe LouisianaLouisiana coastalcoastal parishesparishes ofof VermilionVermilion and and Jefferson Jefferson in in FebruaryFebruary 20182018 andand 2019,2019, respectivelyrespectively (Figure(Figure1 ).1). In In each each year, year, approximately approximately 40% 40% of of the the sampledsampled birdsbirds werewere after after hatch hatch year year (AHY). (AHY). FigureFigure 1.1. Collection sites sites in in Louisiana, Louisiana, USA USA at at parish parish level level and and by by sampling sampling year year for forthis this study: study: (A) (AVermilion,) Vermilion, 2018, 2018, and and (B) ( BJefferson,) Jefferson, 2019. 2019. CollectionCollection sitessites included rice rice fields fields (2018) (2018) and and a acargo cargo ship ship terminal terminal situated situated on onthe theMississippi Mississippi River, River, where where thousands thousands of BBW of BBWDD and andother other waterfowl waterfowl were were observed observed (per- (personalsonal observation, observation, Paul Paul Link, Link, 2019). 2019). Virus Virus isolation isolation (VI) (VI) was was performed performed on on COP COP swabs swabs as aspreviously previously described described [7]. [Viral7]. Viral RNA RNA was extr wasacted extracted (QIAamp (QIAamp Viral RNA Viral Mini RNA Kit, Mini Qiagen Kit, QiagenInc., Valencia, Inc., Valencia, CA, USA) CA, USA)from all from VI-positiv all VI-positivee samples samples following following the manufacturer’s the manufacturer’s rec- recommendation,ommendation, and and tested tested by IAV by IAV matrix matrix real-time real-time reverse reverse transcriptase transcriptase PCR PCR(RRT-PCR) (RRT- PCR)[8]. Whole-genome [8]. Whole-genome sequencing sequencing of IAV-positive of IAV-positive isolates isolates was carried was carried out at outJ. Craig at J. Venter Craig VenterInstitute. Institute. Phylogenetic Phylogenetic analyses analyses were wereconducted conducted using using MEGA MEGA version version 6 [9]; 6 [9 ];the the top top 2 2NCBI NCBI basic basic local local alignment alignment search search tool tool (BLAST (BLAST)) results, based on percentpercent nucleotidenucleotide (nt)(nt) similarity,similarity, werewere chosenchosen onon the the basis basis of of the the criteria criteria that that they they were were from from viruses viruses identified identified from avian species at times predating the query sequence. Sterile blood samples were collected at a total volume less than or equal to 1% of the bird body mass via the brachial
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