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AVIAN PARAMYXOVIRUSES in SHOREBIRDS and Gulls

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AVIAN PARAMYXOVIRUSES in SHOREBIRDS and Gulls journal Diseases, 46(2), 2010, pp. 481-487 \Vildlife Disease Association 2010 AVIAN PARAMYXOVIRUSES IN SHOREBIRDS AND GUllS laura l. Coffee,1,5 Britta A. Hanson,' M. Page Luttrell;' David E. Swa~ne,2 Dennis A. Senne,3 Virginia H. Goekjlan," lawrence J. Niles,4,6 and David E. Stallknecht1, 1 Southeastern Cooperative Wildlife Disease Study, Departrnent of Population Health, College of Veterinary Medicine, The University of Georgia, Athens, Georgia 30602, USA 2 Southeast Poultry Research Laboratory, Agricultural Research Service, US Departrnent of Agriculture, Athens, Georgia 30605, USA 3 US Departrnent of Agriculture, Anirnal and Plant Health Inspection Service, National Veterinary Services Laboratories, Ames, Iowa 50010, USA 4 Endangered and Nongame Species Program, New Jersey Division of Fish and Wildlife, PO Box 400, Trenton, New Jersey 08625, USA 5 Current address: Cornell University, College of Veterinary Medicine, S2-118 Schurman Hall, Biomedical Sciences, Ithaca, New York 14853, USA 6 Current address: Conserve Wildlife Foundation, 516 Farnsworth Avenue, Bordertown, New Jersey 08505, USA 7 Corresponding author (email: [email protected]) ABSTRACT: There are nine serotypes of avian paramyxovirus (APMV), including APMV-1, or Newcastle disease virus. Although free-flying ducks and geese have been extensively monitored for APMV, limited information is available for species in the order Charadriiforrnes. From 2000 to 2005 we tested cloacal swabs from 9,128 shorebirds and gulls (33 species, five families) captured in 10 states within the USA and in three countries in the Caribbean and South America. Avian paramyxoviruses were isolated from 60 (0.7%) samples by inoculation of embryonating chicken eggs; isolates only included APMV-1 and APMV-2. Two isolates (APMV-2) were made from gulls and 58 isolates (APMV-1 [41isolates] and APMV-2 [17 isolates]) were made from shorebirds. All of the positive shorebirds were sampled at Delaware Bay (Delaware and NewJersey) and 45 (78%) of these isolates came from Ruddy Turnstones (Arenaria interpres). The AFMV-1 infection rate was higher among Ruddy Turnstones compared with other shorebird species and varied by year. Avian paramyxovirus-Z was isolated from two of394 (0.5%) Ruddy Turnstones at Delaware Bay in 2001 and from 13 of 735 (1.8%) Ruddy Turnstones during 2002. For both APMV-1 and APMV-2, infection rates were higher among Ruddy Turnstones sampled on the south shore ofDelaware Bay compared to north shore populations, This spatial variation may be related to local movements of Ruddy Turnstones within this ecosystem. The higher prevalence of APMV in Ruddy Turnstones mirrors results observed for avian influenzaviruses in shorebirds and may suggest similar modes of transmission. KEy words: Avian paramyxovirus, Delaware Bay, Red Knot, Ruddy Turnstone, shorebird. INTRODUCTION isolated from wild birds (Stallknecht et al., 1991; Hlinak et al., 2006). Avian paramyxoviruses (APMV) are The occurrence and natural history of negative-strand RNA viruses of the genus APMVs 1-9 are poorly documented in Avulavirus in the family Paramyxoviridae. charadriiform birds, but isolations of The genus includes nine serotypes that APMV-1, -4, and -6 have been reported have been documented in a variety of (Hlinak et al., 2006). Because some of wild, domestic, and pet birds worldwide these birds are highly migratory, crossing (Alexander, 1995). The most economically the equator bi-annually during long mi­ important serotype is APMV-1 (Newcastle grations from winter nesting grounds in disease virus), but other APMV serotypes South America to arctic breeding grounds have been isolated from domestic poultry, (Clark et al., 1993), they present a where they occasionally cause respiratory potential mechanism for the global move­ and reproductive disease (Warke et al., ment of these viruses. To date, domestic 2008). Information about the distribution surveillance in shorebirds has focused of APMVs 2-9 in wild species is limited primarily on avian influenza viruses (Hli­ compared with APMV-1; however, all nine nak et al., 2006). serotypes, except APMV-5, have been Delaware Bay is a major North Amer- 481 482 JOURNAL OF WILDLIFE DISEASES, VOL. 46, NO.2, APRIL 2010 ican stopover site for spring-migrating (Calidris pusilla). Other shorebirds inciden­ shorebirds due to its strategic location tally captured during these efforts were and seasonal abundance ofhorseshoe crab included in this study. With the exception of Sanderlings, birds at Delaware Bay were (Limulus polyphemus) eggs. Aerial surveys sampled in both New Jersey (North shore) of shorebirds during spring migration and Delaware (South shore). Sanderlings were ranked Delaware Bay as the second­ only sampled on the North shore and, during largest stopover site in the Western 2005, sampling of all shorebirds was restricted Hemisphere (Clark et al., 1993). Shore­ to the North shore due to their late arrival and a limited sampling period. birds arrive in poor body condition in mid­ Cloacal samples were collected from cap­ May and spend 2-3 wk rebuilding their tured birds using sterile, cotton-tipped appli­ caloric reserves and body condition for cators (Puritan Medical Products Co., Guil­ breeding (Clark et al., 1993). Due to its ford, Maine, USA) that were placed in sterile, high concentration of migrating shore­ 4-ml cryogenic vials (Corning Inc., Corning, New York, USA) containing 2-3 ml of chilled birds during spring migration, Delaware brain heart infusion broth (Becton, Dickinson Bay represents an ideal sampling site for and Co., Sparks, Maryland, USA) supplement­ investigating avian influenza virus (AIV) ed with 1,000 Ulml penicillin G, 1.0 mg/ml and APMV infections in these species; a streptomycin sulfate, 0.25 mglml gentamicin, high annual prevalence ofAIV infection in 0.50 mglml kanamycin, and 0.025 mglml shorebirds at Delaware Bay, primarily in amphotericin B (Sigma Chemical Company, St. Louis, Missouri, USA). Samples were Ruddy Turnstones (Arenaria interpres), temporarily placed on ice in coolers and has been previously reported (Hanson et transferred into liquid nitrogen at the end of al., 2008). The objectives of this study the sampling event (generally less than 8 hr). were to analyze and report APMV preva­ They remained in liquid nitrogen for 2-21 days lence in shorebirds and gulls at this, and until they were transported to the laboratory and stored at -70 C. other, sites and to determine if the Samples were removed from the freezer, occurrence of these viruses in birds at allowed to thaw at room temperature for 30­ Delaware Bay is species or site related. 40 min, vortexed at high speed for 10 sec, and centrifuged at 1,500 X G for 15 min. From MATERIALS AND METHODS each sample, 0.25 ml was injected into four, specific-pathogen-free, 9-day-old embryonat­ From 2000 to 2005, 9,128 charadriiform ing chicken eggs from the University of birds (including species in families Haernoto­ Georgia's Poultry Disease Research Center dididae, Recurvirostridae, Charadriidae, Sco­ in Athens, Georgia, USA. Eggs were incubated lopacidae, and Laridae) were sampled (Ta­ at 37 C for 5 days, and amnio-allantoic fluid ble 1). These included 6,061 birds from was harvested and tested for hemagglutination . Delaware Bay, 2,360 birds from 10 other (HA). All HA-positive samples were submitted . states (Arkansas, Florida, Georgia, Kansas, to the National Veterinary Services Laborato­ Louisiana, Missouri, Massachusetts, New ries, Veterinary Services, Animal and Plant York, South Carolina, and Texas), and 707 Health Inspection Service, US Department of birds from South America (Argentina and Agriculture for virus serotyping by hemagglu­ Chile) and Bermuda sampled during winter tination inhibition (HI); HA and HI tests were (2001-2002). Collection site, capture tech­ done as described by the Committee on niques, and dates of sampling were described Standard Methods for the Hemagglutination in Hanson et al. (2008). Sampling at Delaware and Hemagglutination Inhibition Test for Bay was conducted in conjunction with Newcastle Disease (1975). banding and surveillance activities conducted Data were analyzed using SAS Software by the Division of Fish and Wildlife of the (SAS Institute Inc., Cary, North Carolina, New Jersey Department of Environmental USA). Virus isolation results were dichoto­ Protection and the Delaware Department of mized for each subtype and set as outcome Natural Resources and Environmental Con­ disease variables. Uniform distribution of trol'. Four species of shorebirds were prefer­ APMV prevalence was tested among popula­ entially sampled: Red Knots (Calidris canu­ tions (by species, geographic location, and tu.s}, Sanderlings (Calidris alba), Ruddy year) using the chi-square goodness-of-fit test, Turnstones, and Semipalmated Sandpipers the Mantel-Haenzel chi-square test, or COFFEE ET AL-APMV IN SHOREBIRDS AND GULLS 483 TABLE 1. Birds sampled and tested for avian paramyxovirus during 2000-2005 at Delaware Bay, USA and other sites. Family Species Charadriidae (n=43) Semipalmated Plover (Charadrius semipalrnatus) 20 Killdeer (Charadrius vociferous) 11 Wilson's Plover (Charadrius wilsonia) 5 Black-bellied Plover (Pluvialis squatarola) 7 Haematopodidae (n=84) American Oystercatcher (Haematopus palliatus) 84 Recurvirostridae (n=6) Black-necked Stilt (Himantopus mexicanus) 6 Scolopacidae (n=7999) Spotted Sandpiper (Actitis macularius) 5 Ruddy Turnstone (Arenaria interpres) 26 (2,368) Sanderling (Calidris alba) 11 (741) Dunlin (Calidris alpina) 137 (378) Red Knot (Calidris canutus)
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