Body condition explains migratory performance of a long-distance migrant.

Body condition (i.e. relative mass after correcting for structural size) affects the behaviour of migrating birds, but how body condition affects migratory performance, timing and fitness is still largely unknown. Here, we studied the effects of relative body condition on individual departure decisions, wind selectivity, flight speed and timing of migration for a long-distance migratory shorebird, the red knot Calidris canutus rufa. By using automated VHF telemetry on a continental scale, we studied knots' migratory movements with unprecedented temporal resolution over a 3-year period. Knots with a higher relative body condition left the staging site later than birds in lower condition, yet still arrived earlier to their Arctic breeding grounds compared to knots in lower relative body condition. They accomplished this by selecting more favourable winds at departure, thereby flying faster and making shorter stops en route Individuals with a higher relative body condition in spring migrated south up to a month later than individuals in lower condition, suggesting that individuals in better condition were more likely to have bred successfully. Moreover, individuals with a lower relative body condition in spring had a lower probability of being detected in autumn, suggestive of increased mortality. The pressure to arrive early to the breeding grounds is considered to be an important constraint of migratory behaviour and this study highlights the important influence of body condition on migratory decisions, performance and potentially fitness of migrant birds.

Influenza A virus: sampling of the unique shorebird habitat at Delaware Bay, USA.

Delaware (DE) Bay, in the northeastern USA, has long been recognized as a hotspot for avian influenza A virus (IAV); every spring, this coastal region serves as a brief stopover site for thousands of long-distance migrating shorebirds, en route to breeding grounds in the Arctic. During these stopovers, IAV has been consistently recovered from ruddy turnstones (Arenaria interpres) that are likely to become infected as they feed by probing sand and cobble in search of food. In May 2010-2012, we successfully isolated 19 IAV from environmental samples (sand, n = 18; horseshoe crab eggs, n = 1) obtained from DE Bay sites. Two of these viruses were subjected to laboratory conditions similar to those in the DE Bay spring-time environment, and remained infectious for 7 days. Here, through the recovery of IAV from environmental samples, temperature monitoring at and below the sand surface and simulated laboratory trials, we provide evidence that the beach environment may enable localized transmission and short-term maintenance of IAV in this unique ecosystem.

Spring Migration Stopover Ecology of Avian Influenza Virus Shorebird Hosts at Delaware Bay.

Although low pathogenicity avian influenza viruses (LPAIV) are detected in shorebirds at Delaware Bay annually, little is known about affected species habitat preferences or the movement patterns that might influence virus transmission and spread. During the 5-wk spring migration stopover period during 2007-2008, we conducted a radiotelemetry study of often-infected ruddy turnstones (Arenaria interpres morinella; n = 60) and rarely infected sanderlings (Calidris alba; n = 20) to identify locations and habitats important to these species (during daytime and nighttime), determine the extent of overlap with other AIV reservoir species or poultry production areas, reveal possible movements of AIV around the Bay, and assess whether long-distance movement of AIV is likely after shorebird departure. Ruddy turnstones and sanderlings both fed on Bay beaches during the daytime. However, sanderlings used remote sandy points and islands during the nighttime while ruddy turnstones primarily used salt marsh harboring waterfowl and gull breeding colonies, suggesting that this environment supports AIV circulation. Shorebird locations were farther from agricultural land and poultry operations than were random locations, suggesting selection away from poultry. Further, there was no areal overlap between shorebird home ranges and poultry production areas. Only 37% (22/60) of ruddy turnstones crossed into Delaware from capture sites in New Jersey, suggesting partial site fidelity and AIV gene pool separation between the states. Ruddy turnstones departed en masse around June 1 when AIV prevalence was low or declining, suggesting that a limited number of birds could disperse AIV onto the breeding grounds. This study provides needed insight into AIV and migratory host ecology, and results can inform both domestic animal AIV prevention and shorebird conservation efforts.

Long-term surveillance of H7 influenza viruses in American wild aquatic birds: are the H7N3 influenza viruses in wild birds the precursors of highly pathogenic strains in domestic poultry?

The emergence of influenza A virus (IAV) in domestic avian species and associated transmissions to mammals is unpredictable. In the Americas, the H7 IAVs are of particular concern, and there have been four separate outbreaks of highly pathogenic (HP) H7N3 in domestic poultry in North and South America between 2002 and 2012, with occasional spillover into humans. Here, we use long-term IAV surveillance in North American shorebirds at Delaware Bay, USA, from 1985 to 2012 and in ducks in Alberta, Canada, from 1976 to 2012 to determine which hemagglutinin (HA)-neuraminidase (NA) combinations predominated in Anseriformes (ducks) and Charadriiformes (shorebirds) and whether there is concordance between peaks of H7 prevalence and transmission in wild aquatic birds and the emergence of H7 IAVs in poultry and humans. Whole-genome sequencing supported phylogenetic and genomic constellation analyses to determine whether HP IAVs emerge in the context of specific internal gene segment sequences. Phylogenetic analysis of whole-genome sequences of the H7N3 influenza viruses from wild birds and HP H7N3 outbreaks in the Americas indicate that each HP outbreak was an independent emergence event and that the low pathogenic (LP) avian influenza precursors were most likely from dabbling ducks. The different polybasic cleavage sites in the four HP outbreaks support independent origins. At the 95% nucleotide percent identity-level phylogenetic analysis showed that the wild duck HA, PB1, and M sequences clustered with the poultry and human outbreak sequences. The genomic constellation analysis strongly suggests that gene segments/virus flow from wild birds to domestic poultry.

Mercury, Lead, Cadmium, Arsenic, Chromium and Selenium in Feathers of Shorebirds during Migrating through Delaware Bay, New Jersey: Comparing the 1990s and 2011/2012.

Understanding temporal changes in contaminant levels in coastal environments requires comparing levels of contaminants from the same species from different time periods, particularly if species are declining. Several species of shorebirds migrating through Delaware Bay have declined from the 1980s to the present. To evaluate some contaminants as cause for the declines, we examine levels of mercury, lead, cadmium, arsenic, chromium and selenium in feathers of red knot (Calidris canutus, N = 46 individuals), semipalmated sandpiper (Calidris pusilla, N = 70) and sanderling (Calidris alba, N = 32) migrating through Delaware Bay, New Jersey, USA, from 1991 to 1992 (N = 40), 1995 (N = 28), and 2011-2012 (N = 80) to determine if levels have changed. We found: (1) arsenic, chromium, and lead increased in red knot and decreased in semipalmated sandpiper; (2) cadmium decreased in semipalmated sandpipers; (3) mercury decreased in red knot and sanderlings; (4) selenium decreased in red knot and increased in semipalmated sandpipers. In 2011/2012 there were significant interspecific differences for arsenic, mercury and selenium. Except for selenium, the element levels were well below levels reported for feathers of other species. The levels in feathers in red knots, sanderling, and semipalmated sandpipers from Delaware Bay in 2011/2012 were well below levels in feathers that are associated with effect levels, except for selenium. Selenium levels ranged from 3.0 µg·g-1 dry weight to 5.8 µg·g-1 (semipalmated sandpiper), within the range known to cause adverse effects, suggesting the need for further examination of selenium levels in birds. The levels of all elements were well below those reported for other marine species, except for selenium, which was near levels suggesting possible toxic effects.

Influenza a virus migration and persistence in North American wild birds.

Wild birds have been implicated in the emergence of human and livestock influenza. The successful prediction of viral spread and disease emergence, as well as formulation of preparedness plans have been hampered by a critical lack of knowledge of viral movements between different host populations. The patterns of viral spread and subsequent risk posed by wild bird viruses therefore remain unpredictable. Here we analyze genomic data, including 287 newly sequenced avian influenza A virus (AIV) samples isolated over a 34-year period of continuous systematic surveillance of North American migratory birds. We use a Bayesian statistical framework to test hypotheses of viral migration, population structure and patterns of genetic reassortment. Our results reveal that despite the high prevalence of Charadriiformes infected in Delaware Bay this host population does not appear to significantly contribute to the North American AIV diversity sampled in Anseriformes. In contrast, influenza viruses sampled from Anseriformes in Alberta are representative of the AIV diversity circulating in North American Anseriformes. While AIV may be restricted to specific migratory flyways over short time frames, our large-scale analysis showed that the long-term persistence of AIV was independent of bird flyways with migration between populations throughout North America. Analysis of long-term surveillance data provides vital insights to develop appropriately informed predictive models critical for pandemic preparedness and livestock protection.

Annual survival of ruddy turnstones is not affected by natural infection with low pathogenicity avian influenza viruses.

The population of ruddy turnstones (Arenaria interpres morinella) that migrates through Delaware Bay has undergone severe declines in recent years, attributable to reduced availability of horseshoe crab (Limulus polyphemus) eggs at this critical spring migration stopover site. Concurrently, this population has experienced annual low pathogenicity avian influenza virus (AIV) epidemics at this same site. Using a prospective cohort study design with birds individually flagged during May-June 2006-2008, we evaluated resighting rates (a proxy for annual survival) between AIV-infected and uninfected birds at 1 yr after capture, testing, and measurement. Overall resighting rate was 46%, which varied by year and increased with relative mass of the bird when captured. Resighting rates were not different between AIV-infected and uninfected birds in any period. In multivariate analyses, infection status was also unrelated to resighting rate after controlling for year, day, state, sex, body size, mass index, or whether the bird was blood-sampled. Thus, apparent annual survival in ruddy turnstones was not reduced by AIV infection at this migratory stopover. However, it is unknown whether intestinal AIV infection might cause subtle reductions in weight gain which could negatively influence reproduction.

Avian influenza virus infection dynamics in shorebird hosts.

To gain insight into avian influenza virus (AIV) transmission, exposure, and maintenance patterns in shorebirds at Delaware Bay during spring migration, we examined temporal AIV prevalence trends in four Charadriiformes species with the use of serial cross-sectional data from 2000 through 2008 and generalized linear and additive models. Prevalence of AIV in Ruddy Turnstones (Arenaria interpres morinella) increased after arrival, peaked in mid-late May, and decreased prior to departure. Antibody prevalence also increased over this period; together, these results suggested local infection and recovery prior to departure. Red Knots (Calidris canutus rufa), Sanderlings (Calidris alba), and Laughing Gulls (Leucophaeus atricilla) were rarely infected, but dynamic changes in antibody prevalence differed among species. In Red Knots, declining antibody prevalence over the stopover period suggested AIV exposure prior to arrival at Delaware Bay with limited infection at this site. Antibody prevalence was consistently high in Laughing Gulls and low in Sanderlings. Both viral prevalence and antibody prevalence in Sanderlings varied directly with those in turnstones, suggesting virus spillover to Sanderlings. Results indicate that, although hundreds of thousands of birds concentrate at Delaware Bay during spring, dynamics of AIV infection differ among species, perhaps due to differences in susceptibility, potential for contact with AIV at this site, or prior exposure. Additionally, Ruddy Turnstones possibly act as a local AIV amplifying host rather than a reservoir.

Avian paramyxoviruses in shorebirds and gulls.

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 Charadriiformes. 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 [41 isolates] and APMV-2 [17 isolates]) were made from shorebirds. All of the positive shorebirds were sampled at Delaware Bay (Delaware and New Jersey) and 45 (78%) of these isolates came from Ruddy Turnstones (Arenaria interpres). The APMV-1 infection rate was higher among Ruddy Turnstones compared with other shorebird species and varied by year. Avian paramyxovirus-2 was isolated from two of 394 (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 of Delaware 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 influenza viruses in shorebirds and may suggest similar modes of transmission.

Coincident ruddy turnstone migration and horseshoe crab spawning creates an ecological 'hot spot' for influenza viruses.

Since 1985, avian influenza virus surveillance has been conducted annually from mid-May to early June in charadriiform species from the families Scolopacidae and Laridae (shorebirds and gulls) at Delaware Bay in the northeast United States. The mass migrations of shorebirds, gulls and horseshoe crabs (Limulus polyphemus) coincide at that time, and large numbers of migrating birds pause at Delaware Bay to feed on horseshoe crab eggs deposited at the high-tide line. Influenza viruses are consistently isolated from charadriiform birds at Delaware Bay, at an overall rate approximately 17 times the combined rate of isolation at all other surveillance sites worldwide (490 isolates/9474 samples, 5.2% versus 49 isolates per 15,848 samples, 0.3%, respectively; Proportion test, p < 0.0001). The likelihood of isolating influenza viruses at Delaware Bay is dependent on the presence of ruddy turnstone (Arenaria interpres) at the sampling site (G-test of independence, p < 0.001). The convergence of host factors and environmental factors results in a unique ecological 'hot spot' for influenza viruses in Charadriiformes.

Rapid population decline in red knots: fitness consequences of decreased refuelling rates and late arrival in Delaware Bay.

Most populations of migrant shorebirds around the world are in serious decline, suggesting that vital condition-dependent rates such as fecundity and annual survival are being affected globally. A striking example is the red knot (Calidris canutus rufa) population wintering in Tierra del Fuego, which undertakes marathon 30,000 km hemispheric migrations annually. In spring, migrant birds forage voraciously on horseshoe crab eggs in Delaware Bay in the eastern USA before departing to breed in Arctic polar deserts. From 1997 to 2002 an increasing proportion of knots failed to reach threshold departure masses of 180-200 g, possibly because of later arrival in the Bay and food shortage from concurrent over-harvesting of crabs. Reduced nutrient storage, especially in late-arriving birds, possibly combined with reduced sizes of intestine and liver during refuelling, had severe fitness consequences for adult survival and recruitment of young in 2000-2002. From 1997 to 2002 known survivors in Delaware Bay were heavier at initial capture than birds never seen again, annual survival of adults decreased by 37% between May 2000 and May 2001, and the number of second-year birds in wintering flocks declined by 47%. Population size in Tierra del Fuego declined alarmingly from 51,000 to 27,000 in 2000-2002, seriously threatening the viability of this subspecies. Demographic modelling predicts imminent endangerment and an increased risk of extinction of the subspecies without urgent risk-averse management.