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) 921 (1,723) White-rumped Sandpiper (Calidris fuscicollis) 116 Stilt Sandpiper (Calidris hirnantopus'i 77 Western Sandpiper (Calidris mauri) 78 Pectoral Sandpiper (Calidris melanotos) 42 Least Sandpiper (Calidris minutilla) 155 (128) Semipalmated Sandpiper (Calidris pusilla) 307 (445) Common Snipe (Gallinago gallinago) 4 Short-billed Dowitcher (Limnodromus griseus) 59 (157) Long-billed Dowitcher (Limnodromus scolopaceus) 58 Marbled Godwit tLimosa jedoa) 11 Hudsonian Godwit (Limosa haemastica) 12 Wilson's Phalarope (Phalaropus tricolor) 4 Lesser Yellowlegs (Tringa fiavipes) 17 Willet (Tringa semipalmatus) 10 (9) Laridae (n=996) Herring Gull (Lams argentatus) 41 (5) Laughing Gull (Lams atricilla) 529 (58) Ring-billed Gull (Lams delawarensis) 194 Great Black-backed Gull (Lams marinus) 6 Black Skimmer (Rynchops niger) 1 (49) Forster's Tern (Sterna [orsteri) 1 Common Tern (Sterna hirundo) 105 Royal Tern iThalasseus maxima) 3 Sandwich Tern iThalasseus sandvicensis) 4 Total 3,067 (6,061)

,a Number of birds sampled outside of Delaware Bay (number of birds sampled at Delaware Bay).

Fischer's exact test as the data required Scolopacidae (n=7,999) were positive for (Cl=O.05). APMV-1, and 17 birds were positive for APMV-2. No isolations of APMV-3 RESULTS through -9 were made. All 58 viruses from Cloacal swabs from birds in families shorebirds were isolated from birds sam­ Charadriidae (n = 43), Haematopodidae pled at Delaware Bay, where 5,949 (n=84), and Recurvirostridae (n=6) were shorebirds were sampled (Table 2). For­ all found negative. Of 996 birds tested in ty-five out of 58 (77%) isolates were from the family Laridae, two Laughing Gulls Ruddy Turnstones, accounting for 30/41 (Larus atricilla), one from Jamaica Bay, (73%) APMV-1 and 15/17 (88%) APMV-2 New York and one from Reed's Beach, isolates, yet this species represented only New Jersey, were positive for APMV-2. 39% of the population sampled at Dela­ Cloacal swabs from 41 birds in the family ware Bay. 484 JOURNAL OF WILDLIFE DISEASES, VOL. 46, NO.2, APRIL 2010

TABLE 2. Number of birds tested, and positive, for two serotypes of avian paramyxovirus (APMV) isolated from shorebirds (family Scolopacidae) at Delaware Bay, 2000-2005 (prevalence given in parentheses).

Species No. tested APMV-1 (%) APMV-2 (%)

Dunlin 378 2 (0.5) 0 Least Sandpiper 128 1 (0.8) 0 Red Knot 1,723 7 (0.4) 0 Ruddy Turnstone 2,368 30 (1.3) 15 (0.6) Sanderling 741 1 (0.1) 1 (0.1) Semipalmated Sandpiper 445 0 1 (0.2) Short-billed Dowitcher 157 0 0 Willet 9 0 0 Total 5,949 41 (0.7) 17 (0.3)

With the exception of the Semipalmat­ Fifteen APMV-2 isolates were identi­ ed Sandpipers, which were captured with fied from Ruddy Turnstones in 2001 (2/ mist nets, our capture frequency for 394 [0.5%]) and 2002 (131735 [1.8%]). Scolopacidae species at Delaware Bay Two additional isolates were obtained reflected their relative abundance at this from a Semipalmated Sandpiper in 2000 site. This was determined by comparing and from a Sanderling in 2002. Prevalence aerial survey data (US Fish and Wildlife of APMV-2 in Ruddy Turnstones in 2002 Service, 2003) with our sample distribu­ seems to represent an unexpected spike in tion which was: Ruddy Turnstones (39%), the APMV-2 infection rate at Delaware Red Knots (28%), Sanderlings (12%), Bay. The following year, 2003, APMV-2 Semipalmated Sandpipers (7%), Dunlins prevalence declined to zero, where it (Calidris alpine; 6%), Short-billed Dow­ remained for the rest of the study period itchers (Lirnnodrornus griseus; 3%) and (Table 4). Least Sandpipers (Calidris minutilla, 2%) Ruddy Turnstones inhabiting the South (X2 goodness of fit statistic=3.65, shore were at a higher risk for APMV-1 P=0.4554). infection than those on the North shore All 41 APMV-1 isolates were obtained (5.3% vs. 1.5% [P=0.0414]). During 2002, from birds at Delaware Bay during 2000­ APMV-2 was isolated from 13/735 (1.8%) 2003 (Table 3). The overall prevalence of Ruddy Turnstones and from 1/245 (0.4%) APMV-1 in Ruddy Turnstones (1.3%) was Sanderlings sampled from South Bower's . greater than in other species (0.35%), with Beach on the South shore. Similar to Significantly higher prevalence estimates APMV-1 data, Ruddy Turnstones on the noted in 2000 (2.0% [P<0.002]), 2002 South shore were more likely to be (0.8% [P=0.0015]), and 2003 (3.6% infected with APMV-2 than were those [P=0.0164]). In 2001, the proportion of on the North shore (2.4% vs. 0.7% Red Knots infected with APMV-l was [P=0.2690]); however, these prevalence higher than for Ruddy Turnstones (0.8% estimates are not significantly different vs. 0.5%), though the small number of statistically. Because infection rates in all positive isolates (n = 7) for that year species other than Ruddy Turnstones precludes statistical testing of the signifi­ were low, data for all years were combined cance of this finding. In 2003, APMV-1 into South or North shore populations. prevalence in Ruddy Turnstones at Dela­ Statistically similar proportions of APMV­ ware Bay peaked at 3.6%; this is signifi­ 1 (0.3% vs. 0.3%) and APMV-2 (0% vs. cantly higher than the prevalence esti­ 0.1 %) prevalence estimates were shared mates for other years (P=0.006-0.0026), by south and north shore populations for except for in 2000 (2.0% [P=0.8177]). species other than Ruddy Turnstones. COFFEE ET AL.-APMV IN SHOREBIRDS AND GULLS 485

TABLE 3. Number of birds tested, and positive, for avian paramyxovirus (APMV) serotype 1 from the South and North shores of Delaware Bay by year, 2000-2005 (prevalence given in parentheses).

Ruddy Turnstones Other shorebirds Year South shore North shore South shore North shore

2000 6/180 (3.3) 0/116 31718 (0.4) 2/454 (0.4) 2001 0/187 2/207 (1.0) 2/312 (0.6) 3/300 (1.0) 2002 5/454 (1.1) 1/281 (0.4) 0/523 0/380 2003 13/246 (5.3) 3/195 (1.5) 0/86 1/140 (0.7) 2004 0/84 0/173 0 0/279 2005 0 0/245 0 0/389 Total 2411,151 (2.1) 6/1,217 (0.5) 5/1,639 (0.3) 6/1,942 (0.3)

DISCUSSION disparity is unknown, but may relate in part to limited bird (especially Ruddy Birds at Delaware Bay were dispropor­ Turnstone) movement across Delaware tionately more likely to be infected with Bay. If this is the case, prevalence APMV than were birds at other locations. differences observed between birds on At Delaware Bay, members of the family the South shore and North shore may Scolopacidae, specifically Ruddy Turn­ reflect differences in prevalence occurring stones, were at the highest risk. Although in individual Ruddy Turnstone flocks that the reported prevalence is higher, this maintain site (North or South shore) same species and site relationship occurs affinity. with AIV in shorebirds (Hanson et al., Because shorebirds generally embark 2008). It is possible that the higher on spring migration as adults, the vast prevalence of both APMV and AIV in this majority of birds sampled in this survey species (compared to other shorebird were adults. Banding data suggest that less species using these same habitats) is than 2% of birds at Delaware Bay are related to increased susceptibility (Men­ juveniles less than 1 yr ofage (Robinson et des et al., 2006), increased exposure due al., 2003). In wild ducks, the prevalence of to variations in feeding strategies, or to AIV and APMV are highest in juveniles, a species-specific utilization of feeding and difference probably explained by in­ roosting habitats (Nettleship, 2000). creased disease susceptibility, or by an The prevalence of infection for both immunologically naive population (Hin­ APMV-1 and APMV-2 was highest in birds shaw et al., 1985; Stallknecht et al., 1991). sampled on the South shore rather than on Hence, there is a possibility that the the North shore. The reason for this prevalence estimates presented by this

TABLE 4. Number of birds tested, and positive, for avian paramyxovirus (APMV) serotype 2 from the South and North shores of Delaware Bay by year, 2000-2005 (prevalence given in parentheses).

Ruddy Turnstones Other shorebirds Year South shore North shore South shore North shore

2000 0/180 0/116 1/718 (0.1) 0/454 2001 0/187 2/207 (1.0) 0/312 0/300 2002 11/454 (2.4) 2/281 (0.7) 1/523 (0.2) 0/380 2003, 0/246 0/195 0/86 0/140 2004 0/84 0/173 0 0/279 2005 0 0/245 0 0/389 Total 11/1,151 (1.0) 411,217 (0.5) 2/1,639 (0.1) 0/1,942 486 JOURNAL OF WILDLIFE DISEASES, VOL. 46, NO.2, APRIL 2010

study may underestimate the true preva­ ACKNOWLEDGMENTS lence in these populations, especially if We thank the many people who contributed infections are more common in juvenile to the capture and testing ofthe birds included shorebirds. Despite this, none of the in this study: P. Atkinson, A. Baker, K. Bennett, A. Berenstein, O. Blank, D. Carter, cloacal swabs from 557 Red Knots sam­ J. Clark, K. Clark, N. Clark, K. Cole, J. pled in South America in the winter of Collazo, A. Dey, C. Dove, A. Farmer, P. Friar, 2001 tested positive for APVM (D'Amico J. Gansowski, S. Gibbs, P. Gonzalez, M. et aI., 2007). Likewise, Red Knots sampled Haramis, B. Hanington, J. Hatch, J. Hewes, in Florida, Georgia, and South Carolina P. Hodgetts, J. Huffman, K. Kalasz, S. Lehnen, J. Lyons, C. Minton, D. Mizrahi, T. (n=365) in 2000 and 2001, which likely Norton, B. Ortego, M. Peck, W. Pitts, R. belong to the "Florida-Atlantic Coast" Porter, H. Sitters, B. Wilcox, and B. Winn. wintering population (Harrington et al., Laboratory technical assistance was provided 2007), were also found negative for APMV­ by J. Beck. Funding for this work was provided 1 and APMV-2. These results suggest that, through Specific Cooperative Agreements 58­ 6612-80023 and 58-6612-2-220 with the like AN, APMV infections in this species Southeast Poultry Research Laboratory, may be site dependent, and at Delaware USDA-ARS and through the continued spon­ Bay these viruses may be locally amplified. sorship of the Southeastern Cooperative Wild­ Isolations of APMV from shorebirds have life Disease Study member states. been reported from Lake Guelpe in Germany and, at this site, APMV-l and -6 LITERATURE CITED were isolated from Dunlin, Common ALEXANDER, D. J. 1995. The epidemiology and Sandpiper (Actitis hypoleucos), Little Stint control ofavian influenza and Newcastle disease. Journal of Comparative Pathology 112: 105-126. (Calidris minuta}, and Ruff (Philomachus CLARK, K. K, L. J. NILES, AND J. BURGER. 1993. pugnax); the reported prevalence was 2.4% Abundance and distribution of migrant shore­ for APMV-l and 1.7% for APMV-6 and, birds in Delaware Bay. Condor 95: 694-705. with the exception of one Common Sand­ COMMITTEE ON STANDARD METHODS FOR THE HEMAG­ piper, all positive birds were juveniles GLUTINATION AND HEMAGGLUTINATION INHIBITION (Hlinak et al., 2006). TESTFOR NEWCASTLE DISEASE. 1975. Hemagglu­ tination and hemagglutination-inhibition test for Further study is needed to understand Newcastle disease virus-microtiter technique. fully the behavior ofthe Ruddy Turnstone, Proceedings American Association of Veterinary some aspect of which may put them at Laboratory Diagnosticians 17: 1-6. increased risk for infection. According to D'AMICO, V. L., M. BERTELLOTTI, A. J. BAKER, AND L. A. DIAZ. 2007. Exposure of red knots (Calidris Clark et al. (1993), Ruddy Turnstones canutus rufa) to select avian pathogens; Patago­ show similar geographic and temporal nia, Argentina. Journal of Wildlife Diseases 43: -distributions as do Red Knots, and while 794--797. numbers of Ruddy Turnstones observed at HARRINGTON, B. A., B. WINN, AND S. C. BROWN. 2007. Delaware Bay declined substantially in Molt and body mass of red knots in the eastern United States. Wilson Journal of Ornithology 2006, they were still far more abundant 119: 35-42. than Red Knots (Niles et al., 2009). Based HANSON, B. A., M. P. LUTTRELL, V. H. GOEKJIAN, L. on relative abundance, Ruddy Turnstones NILES, D. K SWAYNE, D. A. SENNE, AND D. K may represent a potential sentinel species STALLKNECHT. 2008. Is the occurrence of avian for surveillance directed at pathogens that influenza virus in Charadriiformes species and location dependent? Journal ofWildlife Diseases could impact other threatened or endan­ 44: 351-361. gered shorebird species. However, as HINSHAW, V. S., J. M. WOOD, R. G. VIEBSTEH, R. demonstrated in this survey with APMV, DEIBEL, AND B. TURNER. 1985. Circulation of and in the previous AIV survey (Hanson et influenza viruses and paramyxoviruses in water­ al., ~2008), species-related differences in fowl originating from two different areas of North America. Bulletin of the World Health infection rates commonly occur even with Organization 63: 711-719. closely related and cohabitating shorebird HLINAK, A., R. U. MUHLE, O. WERNER, A. GLOBIG, K species. STARICK, H. SCHIRRMEIER, B. HOFFMANN, A. COFFEE ET AL.-APMV IN SHOREBIRDS AND GULLS 487

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