Negligible evidence for detrimental effects of Leucocytozoon infections among Emperor Geese (Anser canagicus) breeding on the Yukon-Kuskokwim Delta, Alaska.

Emperor Geese (Anser canagicus) are iconic waterfowl endemic to Alaska and adjacent areas of northeastern Russia that are considered to be near threatened by the International Union for Conservation. This species has been identified as harboring diverse viruses and parasites which have, at times, been associated with disease in other avian taxa. To better assess if disease represents a vulnerability for Emperor Geese breeding on the Yukon-Kuskokwim Delta, Alaska, we evaluated if haemosporidian parasites were associated with decreased mass or survival among adult female nesting birds captured during 2006-2016. Through molecular analyses, we detected genetically diverse Leucocytozoon, Haemoproteus, and Plasmodium parasites in 28%, 1%, and 1% of 607 blood samples screened in triplicate, respectively. Using regression analysis, we found evidence for a small effect of Leucocytozoon infection on the mass of incubating adult female Emperor Geese. The estimated mass of infected individuals was approximately 43 g (95% CI: 20-67 g), or approximately 2%, less than uninfected birds when captured during the second half of incubation (days 11-25). We did not, however, find support for an effect of Leucocytozoon infection on survival of adult female nesting Emperor Geese using a multi-state hidden Markov framework to analyze mark-resight and recapture data. Using parasite mitochondrial DNA cytochrome b sequences, we identified 23 haplotypes among infected Emperor Geese. Leucocytozoon haplotypes clustered into three phylogenetically supported clades designated as 'L. simondi clade A', 'L. simondi clade B', and 'other Leucocytozoon'. We did not find evidence that parasites assigned to any of these clades were associated with differential mass measures among nesting adult female Emperor Geese. Collectively, our results provide negligible evidence for Leucocytozoon parasites as causing detrimental effects to adult female Emperor Geese breeding on the Yukon-Kuskokwim Delta.

ASSESSMENT OF VARIATION IN THE DETECTION AND PREVALENCE OF BLOOD PARASITES AMONG SYMPATRICALLY BREEDING GEESE IN WESTERN ALASKA, USA.

Haemosporidian parasites may impact avian health and are subject to shifts in distribution and abundance with changing ecologic conditions. Therefore, understanding variation in parasite prevalence is important for evaluating biologically meaningful changes in infection patterns and associated population level impacts. Previous research in western Alaska, US, indicated a possible increase in Leucocytozoon spp. infection between Emperor Geese (Anser canagicus) sampled in 1996 (<1%, n=134) and during 2011-12 (19.9%, 95% confidence interval [CI]: 3.0-36.8%, n=77); however, different detection methods were used for these estimates. Prior research in this same region identified a lack of Leucocytozoon spp. parasites (0%, n=117) in sympatrically breeding Cackling Geese (Branta hutchinsii minima) in 2011. We molecularly screened blood samples collected from sympatrically breeding Emperor and Cackling Geese in western Alaska during additional breeding seasons to better assess temporal and species-specific variation in the prevalence of blood parasites. We found similar prevalence estimates for Leucocytozoon spp. parasites in Emperor Goose blood samples collected in 1998 and 2014, suggesting consistent infection of Emperor Geese with blood parasites at these time points. Using samples from sympatric geese sampled during 2014, we found evidence for a higher incidence of parasites among Emperor Geese (20.3%, 95% CI: 11.8-32.7%) compared to Cackling Geese (3.6%, 95% CI: 1.1-11.0%), reinforcing the previous finding of species-specific differences in infection. Furthermore, we detected Leucocytozoon, Haemoproteus, and Plasmodium spp. blood parasites in unflighted goslings of both species, supporting the possible transmission of these parasites at western Alaska breeding grounds. Our results help to clarify that prevalence of Leucocytozoon spp. parasites have probably remained consistent among Emperor Geese breeding in western Alaska since the late 1990s and that this species may disproportionally harbor Leucocytozoon spp. compared to sympatrically breeding Cackling Geese.

Synthesis of Maternal Transfer of Mercury in Birds: Implications for Altered Toxicity Risk.

Maternal transfer is a predominant route of methylmercury (MeHg) exposure to offspring. We reviewed and synthesized published and unpublished data on maternal transfer of MeHg in birds. Using paired samples of females' blood (n = 564) and their eggs (n = 1814) from 26 bird species in 6 taxonomic orders, we conducted a meta-analysis to evaluate whether maternal transfer of MeHg to eggs differed among species and caused differential toxicity risk to embryos. Total mercury (THg) concentrations in eggs increased with maternal blood THg concentrations; however, the proportion of THg transferred from females to their eggs differed among bird taxa and with maternal THg exposure. Specifically, a smaller proportion of maternal THg was transferred to eggs with increasing female THg concentrations. Additionally, the proportion of THg that was transferred to eggs at the same maternal blood THg concentration differed among taxonomic orders, with waterfowl (Anseriformes) transferring up to 382% more THg into their eggs than songbirds (Passeriformes). We provide equations to predict THg concentrations in eggs using female blood THg concentrations, and vice versa, which may help translate toxicity benchmarks across tissues and life stages. Our results indicate that toxicity risk of MeHg can vary among bird taxa due to differences in maternal transfer of MeHg to offspring.

Changes in behavior are unable to disrupt a trophic cascade involving a specialist herbivore and its food plant.

Changes in ecological conditions can induce changes in behavior and demography of wild organisms, which in turn may influence population dynamics. Black brant (Branta bernicla nigricans) nesting in colonies on the Yukon-Kuskokwim Delta (YKD) in western Alaska have declined substantially (~50%) since the turn of the century. Black brant are herbivores that rely heavily on Carex subspathacea (Hoppner's sedge) during growth and development. The availability of C. subspathacea affects gosling growth rates, which subsequently affect pre- and postfledging survival, as well as size and breeding probability as an adult. We predicted that long-term declines in C. subspathacea have affected gosling growth rates, despite the potential of behavior to buffer changes in food availability during brood rearing. We used Bayesian hierarchical mixed-effects models to examine long-term (1987-2015) shifts in brant behavior during brood rearing, forage availability, and gosling growth rates at the Tutakoke River colony. We showed that locomotion behaviors have increased (ß = 0.05, 95% CRI: 0.032-0.068) while resting behaviors have decreased (ß = -0.024, 95% CRI: -0.041 to -0.007), potentially in response to long-term shifts in forage availability and brood density. Concurrently, gosling growth rates have decreased substantially (ß = -0.100, 95% CRI: -0.191 to -0.016) despite shifts in behavior, mirroring long-term declines in the abundance of C. subspathacea (ß = -0.191, 95% CRI: -0.355 to -0.032). These results have important implications for individual fitness and population viability, where shifts in gosling behavior putatively fail to mitigate long-term declines in forage availability.

Emperor geese (Anser canagicus) are exposed to a diversity of influenza A viruses, are infected during the non-breeding period and contribute to intercontinental viral dispersal.

Emperor geese (Anser canagicus) are endemic to coastal areas within Beringia and have previously been found to have antibodies to or to be infected with influenza A viruses (IAVs) in Alaska. In this study, we use virological, serological and tracking data to further elucidate the role of emperor geese in the ecology of IAVs in Beringia during the non-breeding period. Specifically, we assess evidence for: (a) active IAV infection during spring staging, autumn staging and wintering periods; (b) infection with novel Eurasian-origin or interhemispheric reassortant viruses; (c) contemporary movement of geese between East Asia and North America; (d) previous exposure to viruses of 14 haemagglutinin subtypes, including Eurasian lineage highly pathogenic (HP) H5 IAVs; and (e) subtype-specific antibody seroconversion and seroreversion. Emperor geese were found to shed IAVs, including interhemispheric reassortant viruses, throughout the non-breeding period; migrate between Alaska and the Russian Far East prior to and following remigial moult; have antibodies reactive to a diversity of IAVs including, in a few instances, Eurasian lineage HP H5 IAVs; and exhibit relatively broad and stable patterns of population immunity among breeding females. Results of this study suggest that emperor geese may play an important role in the maintenance and dispersal of IAVs within Beringia during the non-breeding period and provide information that may be used to further optimize surveillance activities focused on the early detection of Eurasian-origin IAVs in North America.

Migratory goose arrival time plays a larger role in influencing forage quality than advancing springs in an Arctic coastal wetland.

With warmer springs, herbivores migrating to Arctic breeding grounds may experience phenological mismatches between their energy demands and the availability of high quality forage. Yet, how the timing of the start of the season and herbivore arrival influences forage quality is often unknown. In coastal western Alaska, approximately one million migratory geese arrive each spring to breed, where foliar %N and C:N ratios are linked to gosling survival and population growth. We conducted a three-year experiment where we manipulated the start of the growing season using warming chambers and grazing times using captive Pacific black brant (Branta bernicla nigricans) to examine how the timing of these events influences the quality of an important forage species. Our results suggest that grazing timing plays a much greater role than an advanced growing season in determining forage quality. All top models included grazing timing, and suggested that compared to typical grazing timing, early grazing significantly reduced foliar %C by 6% and C:N ratios by 16%, while late goose grazing significantly reduced foliar %N by 15% and increased foliar C:N ratios by 21%. While second-ranking top models included the effect of season, the advanced growing season effect was not significant and only reduced %N by 4%, increased %C by <1%, and increased C:N ratios by 5% compared to an ambient growing season. In summary, in years where geese arrive early, they will consume higher quality forage when they arrive and throughout the season, while in years that geese arrive late they will consume lower quality forage when they arrive and for the remainder of the season. When the growing season starts has only a minor influence on this pattern. Our findings suggest that cues determining migration and arrival times to breeding areas are important factors influencing forage quality for geese in western Alaska.

Serologic Evidence for Influenza A Virus Exposure in Three Loon Species Breeding in Alaska, USA.

Limited information exists about exposure to influenza A viruses (IAVs) in many wild waterbird species, including loons. We analyzed serum samples from breeding adult Pacific (Gavia pacifica), Red-throated (Gavia stellata), and Yellow-billed (Gavia adamsii) loons sampled at three locations along the coast of Alaska, US from 2008 to 2017 to gain a better understanding of the potential role loons play in IAV ecology. We screened loon sera for IAV antibodies using three tests-blocking enzyme-linked immunosorbent assay (bELISA), agar gel immunodiffusion (AGID), and hemagglutination inhibition (HI)-and examined patterns in seroprevalence among species and sampling locations. We found evidence of IAV infection in all loon species and at all breeding locations, although concordance was imperfect among serological tests. Diagnostic tests yielded seroprevalence estimates of 24% (42/172) with bELISA, 8% (5/60) with AGID, and 6% (4/70) with HI. The IAV subtypes to which loon sera reacted using HI were consistent with those detected in waterfowl and gulls at other locations in Alaska, suggesting that loons may be exposed to IAV maintained in sympatric waterbirds. Our study provided evidence that loons inhabiting Alaska were exposed to IAV. However, given imperfect concordance among serologic tests, and relatively low seroprevalence as compared to other avian taxa exposed to IAV in Alaska, they make poor IAV surveillance targets.

Delayed herbivory by migratory geese increases summer-long CO2 uptake in coastal western Alaska.

The advancement of spring and the differential ability of organisms to respond to changes in plant phenology may lead to "phenological mismatches" as a result of climate change. One potential for considerable mismatch is between migratory birds and food availability in northern breeding ranges, and these mismatches may have consequences for ecosystem function. We conducted a three-year experiment to examine the consequences for CO2 exchange of advanced spring green-up and altered timing of grazing by migratory Pacific black brant in a coastal wetland in western Alaska. Experimental treatments represent the variation in green-up and timing of peak grazing intensity that currently exists in the system. Delayed grazing resulted in greater net ecosystem exchange (NEE) and gross primary productivity (GPP), while early grazing reduced CO2 uptake with the potential of causing net ecosystem carbon (C) loss in late spring and early summer. Conversely, advancing the growing season only influenced ecosystem respiration (ER), resulting in a small increase in ER with no concomitant impact on GPP or NEE. The experimental treatment that represents the most likely future, with green-up advancing more rapidly than arrival of migratory geese, results in NEE changing by 1.2 µmol m-2  s-1 toward a greater CO2 sink in spring and summer. Increased sink strength, however, may be mitigated by early arrival of migratory geese, which would reduce CO2 uptake. Importantly, while the direct effect of climate warming on phenology of green-up has a minimal influence on NEE, the indirect effect of climate warming manifest through changes in the timing of peak grazing can have a significant impact on C balance in northern coastal wetlands. Furthermore, processes influencing the timing of goose migration in the winter range can significantly influence ecosystem function in summer habitats.

Evidence for Haemosporidian Parasite Infections in Spectacled Eiders ( Somateria fischeri) Sampled in Alaska, USA during the Breeding Season.

We assessed hematozoa infection in Spectacled Eiders ( Somateria fischeri) at two areas in Alaska, US. No Haemoproteus or Plasmodium species were detected. Leucocytozoon prevalence was 6.5% for adults across sites and 41.9% for juveniles sampled in the Arctic, providing evidence for local transmission. All Leucocytozoon haplotypes were previously detected in waterfowl.

International migration patterns of Red-throated Loons (Gavia stellata) from four breeding populations in Alaska.

Identifying post-breeding migration and wintering distributions of migratory birds is important for understanding factors that may drive population dynamics. Red-throated Loons (Gavia stellata) are widely distributed across Alaska and currently have varying population trends, including some populations with recent periods of decline. To investigate population differentiation and the location of migration pathways and wintering areas, which may inform population trend patterns, we used satellite transmitters (n = 32) to describe migration patterns of four geographically separate breeding populations of Red-throated Loons in Alaska. On average (± SD) Red-throated Loons underwent long (6,288 ± 1,825 km) fall and spring migrations predominantly along coastlines. The most northern population (Arctic Coastal Plain) migrated westward to East Asia and traveled approximately 2,000 km farther to wintering sites than the three more southerly populations (Seward Peninsula, Yukon-Kuskokwim Delta, and Copper River Delta) which migrated south along the Pacific coast of North America. These migration paths are consistent with the hypothesis that Red-throated Loons from the Arctic Coastal Plain are exposed to contaminants in East Asia. The three more southerly breeding populations demonstrated a chain migration pattern in which the more northerly breeding populations generally wintered in more northerly latitudes. Collectively, the migration paths observed in this study demonstrate that some geographically distinct breeding populations overlap in wintering distribution while others use highly different wintering areas. Red-throated Loon population trends in Alaska may therefore be driven by a wide range of effects throughout the annual cycle.

Antibiotic-Resistant Escherichia coli in Migratory Birds Inhabiting Remote Alaska.

We explored the abundance of antibiotic-resistant Escherichia coli among migratory birds at remote sites in Alaska and used a comparative approach to speculate on plausible explanations for differences in detection among species. At a remote island site, we detected antibiotic-resistant E. coli phenotypes in samples collected from glaucous-winged gulls (Larus glaucescens), a species often associated with foraging at landfills, but not in samples collected from black-legged kittiwakes (Rissa tridactyla), a more pelagic gull that typically inhabits remote areas year-round. We did not find evidence for antibiotic-resistant E. coli among 347 samples collected primarily from waterfowl at a second remote site in western Alaska. Our results provide evidence that glaucous-winged gulls may be more likely to be infected with antibiotic-resistant E. coli at remote breeding sites as compared to sympatric black-legged kittiwakes. This could be a function of the tendency of glaucous-winged gulls to forage at landfills where antibiotic-resistant bacterial infections may be acquired and subsequently dispersed. The low overall detection of antibiotic-resistant E. coli in migratory birds sampled at remote sites in Alaska is consistent with the premise that anthropogenic inputs into the local environment or the relative lack thereof influences the prevalence of antibiotic-resistant bacteria among birds inhabiting the area.

Reference Intervals for Serum Biochemistries of Molting Pacific Black Brant ( Branta bernicla nigricans) in Northern Alaska, USA.

We determined reference intervals for nine serum biochemistries in samples from 329 molting, after-hatch-year, Pacific Black Brant ( Branta bernicla nigricans) in Alaska, US. Cholesterol and nonesterified fatty acids differed by sex, but no other differences were noted.

Blood selenium concentrations in female Pacific black brant molting in Arctic Alaska: Relationships with age and habitat salinity.

Blood samples collected from 81 female Pacific black brant (Branta bernicla nigricans) molting near Teshekpuk Lake, Alaska, were analyzed for selenium concentration. The concentration of selenium in blood of after second year (hatched two or more years ago) females (0.84µg/g wet weight) was significantly greater than the concentration in second year (hatched the previous year) females (0.61µg/g wet weight). The concentrations of selenium we found in blood of black brant were 1.5 to 2 times greater than baseline values typical of freshwater birds, but considerably lower than reported in other marine waterfowl sampled in Alaska. This finding may be attributable in part to the nearly exclusive herbivorous diet of black brant. No relationship was noted between blood selenium concentration and molting habitat salinity. We are unaware of any previous reports of blood selenium concentrations in black brant.

Evidence for the exchange of blood parasites between North America and the Neotropics in blue-winged teal (Anas discors).

Blue-winged teal (Anas discors) are abundant, small-bodied dabbling ducks that breed throughout the prairies of the northcentral USA and central Canada and that winter in the southern USA and northern Neotropics. Given the migratory tendencies of this species, it is plausible that blue-winged teal may disperse avian pathogens, such as parasites causing avian malaria, between spatially distant areas. To test the hypothesis that blue-winged teal play a role in the exchange of blood parasites between North America and areas further south, we collected information on migratory tendencies of this species and sampled birds at spatially distant areas during breeding and non-breeding periods to diagnose and genetically characterize parasitic infections. Using a combination of band recovery data, satellite telemetry, molecular diagnostics, and genetic analyses, we found evidence for (1) migratory connectivity of blue-winged teal between our sampling locations in the Canadian prairies and along the US Gulf Coast with areas throughout the northern Neotropics, (2) parasite acquisition at both breeding and non-breeding areas, (3) infection of blue-winged teal sampled in Canada and the USA with Plasmodium parasite lineages associated with the Neotropics, and (4) infection of blue-winged teal with parasites that were genetically related to those previously reported in waterfowl in both North America and South America. Collectively, our results suggest that blue-winged teal likely play a role in the dispersal of blood parasites between the Neotropics and North America, and therefore, the targeting of this species in surveillance programs for the early detection of Neotropical-origin avian pathogens in the USA may be informative.

Trophic dynamics of shrinking Subarctic lakes: naturally eutrophic waters impart resilience to rising nutrient and major ion concentrations.

Shrinking lakes were recently observed for several Arctic and Subarctic regions due to increased evaporation and permafrost degradation. Along with lake drawdown, these processes often boost aquatic chemical concentrations, potentially impacting trophic dynamics. In particular, elevated chemical levels may impact primary productivity, which may in turn influence populations of primary and secondary consumers. We examined trophic dynamics of 18 shrinking lakes of the Yukon Flats, Alaska, that had experienced pronounced increases in nutrient (>200 % total nitrogen, >100 % total phosphorus) and ion concentrations (>100 % for four major ions combined) from 1985-1989 to 2010-2012, versus 37 stable lakes with relatively little chemical change over the same period. We found that phytoplankton stocks, as indexed by chlorophyll concentrations, remained unchanged in both shrinking and stable lakes from the 1980s to 2010s. Moving up the trophic ladder, we found significant changes in invertebrate abundance across decades, including decreased abundance of five of six groups examined. However, these decadal losses in invertebrate abundance were not limited to shrinking lakes, occurring in lakes with stable surface areas as well. At the top of the food web, we observed that probabilities of lake occupancy for ten waterbird species, including adults and chicks, remained unchanged from the period 1985-1989 to 2010-2012. Overall, our study lakes displayed a high degree of resilience to multi-trophic cascades caused by rising chemical concentrations. This resilience was likely due to their naturally high fertility, such that further nutrient inputs had little impact on waters already near peak production.

Evidence for intercontinental parasite exchange through molecular detection and characterization of haematozoa in northern pintails (Anas acuta) sampled throughout the North Pacific Basin.

Empirical evidence supports wild birds as playing a role in the interhemispheric exchange of bacteria and viruses; however, data supporting the redistribution of parasites among continents are limited. In this study, the hypothesis that migratory birds contribute to the redistribution of parasites between continents was tested by sampling northern pintails (Anas acuta) at locations throughout the North Pacific Basin in North America and East Asia for haemosporidian infections and assessing the genetic evidence for parasite exchange. Of 878 samples collected from birds in Alaska (USA), California (USA), and Hokkaido (Japan) during August 2011-May 2012 and screened for parasitic infections using molecular techniques, Leucocytozoon, Haemoproteus, and Plasmodium parasites were detected in 555 (63%), 44 (5%), and 52 (6%) samples, respectively. Using an occupancy modeling approach, the probability of detecting parasites via replicate genetic tests was estimated to be high (ρ > 0.95). Multi-model inference supported variation of Leucocytozoon parasite prevalence by northern pintail age class and geographic location of sampling in contrast to Haemoproteus and Plasmodium parasites for which there was only support for variation in parasite prevalence by sampling location. Thirty-one unique mitochondrial DNA haplotypes were detected among haematozoa infecting northern pintails including seven lineages shared between samples from North America and Japan. The finding of identical parasite haplotypes at widely distributed geographic locations and general lack of genetic structuring by continent in phylogenies for Leucocytozoon and Plasmodium provides evidence for intercontinental genetic exchange of haemosporidian parasites. Results suggest that migratory birds, including waterfowl, could therefore facilitate the introduction of avian malaria and other haemosporidia to novel hosts and spatially distant regions.

Pronounced chemical response of Subarctic lakes to climate-driven losses in surface area.

Losses in lake area have been observed for several Arctic and Subarctic regions in recent decades, with unknown consequences for lake ecosystems. These reductions are primarily attributed to two climate-sensitive mechanisms, both of which may also cause changes in water chemistry: (i) increased imbalance of evaporation relative to inflow, whereby increased evaporation and decreased inflow act to concentrate solutes into smaller volumes; and (ii) accelerated permafrost degradation, which enhances sublacustrine drainage while simultaneously leaching previously frozen solutes into lakes. We documented changes in nutrients [total nitrogen (TN), total phosphorus (TP)] and ions (calcium, chloride, magnesium, sodium) over a 25 year interval in shrinking, stable, and expanding Subarctic lakes of the Yukon Flats, Alaska. Concentrations of all six solutes increased in shrinking lakes from 1985-1989 to 2010-2012, while simultaneously undergoing little change in stable or expanding lakes. This created a present-day pattern, much weaker or absent in the 1980s, in which shrinking lakes had higher solute concentrations than their stable or expanding counterparts. An imbalanced evaporation-to-inflow ratio (E/I) was the most likely mechanism behind such changes; all four ions, which behave semiconservatively and are prone to evapoconcentration, increased in shrinking lakes and, along with TN and TP, were positively related to isotopically derived E/I estimates. Moreover, the most conservative ion, chloride, increased >500% in shrinking lakes. Conversely, only TP concentration was related to probability of permafrost presence, being highest at intermediate probabilities. Overall, the substantial increases of nutrients (TN >200%, TP >100%) and ions (>100%) may shift shrinking lakes towards overly eutrophic or saline states, with potentially severe consequences for ecosystems of northern lakes.

Multi-trophic resilience of boreal lake ecosystems to forest fires.

Fires are the major natural disturbance in the boreal forest, and their frequency and intensity will likely increase as the climate warms. Terrestrial nutrients released by fires may be transported to boreal lakes, stimulating increased primary productivity, which may radiate through multiple trophic levels. Using a before-after-control-impact (BACI) design, with pre- and postfire data from burned and unburned areas, we examined effects of a natural fire across several trophic levels of boreal lakes, from nutrient and chlorophyll levels, to macroinvertebrates, to waterbirds. Concentrations of total nitrogen and phosphorus were not affected by the fire. Chlorophyll a levels were also unaffected, likely reflecting the stable nutrient concentrations. For aquatic invertebrates, we found that densities of three functional feeding groups did not respond to the fire (filterers, gatherers, scrapers), while two groups increased (shredders, predators). Amphipods accounted for 98% of shredder numbers, and we hypothesize that fire-mediated habitat changes may have favored their generalist feeding and habitat ecology. This increase in amphipods may, in turn, have driven increased predator densities, as amphipods were the most numerous invertebrate in our lakes and are commonly taken as prey. Finally, abundance of waterbird young, which feed primarily on aquatic invertebrates, was not affected by the fire. Overall, ecosystems of our study lakes were largely resilient to forest fires, likely due to their high initial nutrient concentrations and small catchment sizes. Moreover, this resilience spanned multiple trophic levels, a significant result for ecologically similar boreal regions, especially given the high potential for increased fires with future climate change.

Genomic analysis of avian influenza viruses from waterfowl in western Alaska, USA.

The Yukon-Kuskokwim Delta (Y-K Delta) in western Alaska is an immense and important breeding ground for waterfowl. Migratory birds from the Pacific Americas, Central Pacific, and East Asian-Australasian flyways converge in this region, providing opportunities for intermixing of North American- and Eurasian-origin hosts and infectious agents, such as avian influenza virus (AIV). We characterized the genomes of 90 low pathogenic (LP) AIV isolates from 11 species of waterfowl sampled on the Y-K Delta between 2006 and 2009 as part of an interagency surveillance program for the detection of the H5N1 highly pathogenic (HP) strain of AIV. We found evidence for subtype and genetic differences between viruses from swans and geese, dabbling ducks, and sea ducks. At least one gene segment in 39% of all isolates was Eurasian in origin. Target species (those ranked as having a relatively high potential to introduce HP H5N1 AIV to North America) were no more likely than nontarget species to carry viruses with genes of Eurasian origin. These findings provide evidence that the frequency at which viral gene segments of Eurasian origin are detected does not result from a strong species effect, but rather we suspect it is linked to the geographic location of the Y-K Delta in western Alaska where flyways from different continents overlap. This study provides support for retaining the Y-K Delta as a high priority region for the surveillance of Asian avian pathogens such as HP H5N1 AIV.

High seroprevalence of antibodies to avian influenza viruses among wild waterfowl in Alaska: implications for surveillance.

We examined seroprevalence (presence of detectable antibodies in serum) for avian influenza viruses (AIV) among 4,485 birds, from 11 species of wild waterfowl in Alaska (1998-2010), sampled during breeding/molting periods. Seroprevalence varied among species (highest in eiders (Somateria and Polysticta species), and emperor geese (Chen canagica)), ages (adults higher than juveniles), across geographic locations (highest in the Arctic and Alaska Peninsula) and among years in tundra swans (Cygnus columbianus). All seroprevalence rates in excess of 60% were found in marine-dependent species. Seroprevalence was much higher than AIV infection based on rRT-PCR or virus isolation alone. Because pre-existing AIV antibodies can infer some protection against highly pathogenic AIV (HPAI H5N1), our results imply that some wild waterfowl in Alaska could be protected from lethal HPAIV infections. Seroprevalence should be considered in deciphering patterns of exposure, differential infection, and rates of AIV transmission. Our results suggest surveillance programs include species and populations with high AIV seroprevalences, in addition to those with high infection rates. Serologic testing, including examination of serotype-specific antibodies throughout the annual cycle, would help to better assess spatial and temporal patterns of AIV transmission and overall disease dynamics.