Flyway structure in the circumpolar greater white-fronted goose.

Dispersal and migratory behavior are influential factors in determining how genetic diversity is distributed across the landscape. In migratory species, genetic structure can be promoted via several mechanisms including fidelity to distinct migratory routes. Particularly within North America, waterfowl management units have been delineated according to distinct longitudinal migratory flyways supported by banding data and other direct evidence. The greater white-fronted goose (Anser albifrons) is a migratory waterfowl species with a largely circumpolar distribution consisting of up to six subspecies roughly corresponding to phenotypic variation. We examined the rangewide population genetic structure of greater white-fronted geese using mtDNA control region sequence data and microsatellite loci from 23 locales across North America and Eurasia. We found significant differentiation in mtDNA between sampling locales with flyway delineation explaining a significant portion of the observed genetic variation (~12%). This is concordant with band recovery data which shows little interflyway or intercontinental movements. However, microsatellite loci revealed little genetic structure suggesting a panmictic population across most of the Arctic. As with many high-latitude species, Beringia appears to have played a role in the diversification of this species. A common Beringian origin of North America and Asian populations and a recent divergence could at least partly explain the general lack of structure at nuclear markers. Further, our results do not provide strong support for the various taxonomic proposals for this species except for supporting the distinctness of two isolated breeding populations within Cook Inlet, Alaska (A. a. elgasi) and Greenland (A. a. flavirostris), consistent with their subspecies status.

Genetic structure among greater white-fronted goose populations of the Pacific Flyway.

An understanding of the genetic structure of populations in the wild is essential for long-term conservation and stewardship in the face of environmental change. Knowledge of the present-day distribution of genetic lineages (phylogeography) of a species is especially important for organisms that are exploited or utilize habitats that may be jeopardized by human intervention, including climate change. Here, we describe mitochondrial (mtDNA) and nuclear genetic (microsatellite) diversity among three populations of a migratory bird, the greater white-fronted goose (Anser albifrons), which breeds discontinuously in western and southwestern Alaska and winters in the Pacific Flyway of North America. Significant genetic structure was evident at both marker types. All three populations were differentiated for mtDNA, whereas microsatellite analysis only differentiated geese from the Cook Inlet Basin. In sexual reproducing species, nonrandom mate selection, when occurring in concert with fine-scale resource partitioning, can lead to phenotypic and genetic divergence as we observed in our study. If mate selection does not occur at the time of reproduction, which is not uncommon in long-lived organisms, then mechanisms influencing the true availability of potential mates may be obscured, and the degree of genetic and phenotypic diversity may appear incongruous with presumed patterns of gene flow. Previous investigations revealed population-specific behavioral, temporal, and spatial mechanisms that likely influence the amount of gene flow measured among greater white-fronted goose populations. The degree of observed genetic structuring aligns well with our current understanding of population differences pertaining to seasonal movements, social structure, pairing behavior, and resource partitioning.

Chewing Lice of Swan Geese (Anser cygnoides): New Host-Parasite Associations.

Chewing lice (Phthiraptera) that parasitize the globally threatened swan goose Anser cygnoides have been long recognized since the early 19th century, but those records were probably biased towards sampling of captive or domestic geese due to the small population size and limited distribution of its wild hosts. To better understand the lice species parasitizing swan geese that are endemic to East Asia, we collected chewing lice from 14 wild geese caught at 3 lakes in northeastern Mongolia. The lice were morphologically identified as 16 Trinoton anserinum (Fabricius, 1805), 11 Ornithobius domesticus Arnold, 2005, and 1 Anaticola anseris (Linnaeus, 1758). These species are known from other geese and swans, but all of them were new to the swan goose. This result also indicates no overlap in lice species between older records and our findings from wild birds. Thus, ectoparasites collected from domestic or captive animals may provide biased information on the occurrence, prevalence, host selection, and host-ectoparasite interactions from those on wild hosts.

Demographic outcomes of diverse migration strategies assessed in a metapopulation of tundra swans.

BACKGROUND: Migration is a prominent aspect of the life history of many avian species, but the demographic consequences of variable migration strategies have only infrequently been investigated, and rarely when using modern technological and analytical methods for assessing survival, movement patterns, and long-term productivity in the context of life history theory. We monitored the fates of 50 satellite-implanted tundra swans (Cygnus columbianus) over 4 years from five disparate breeding areas in Alaska, and used known-fate analyses to estimate monthly survival probability relative to migration distance, breeding area, migratory flyway, breeding status, and age. We specifically tested whether migratory birds face a trade-off, whereby long-distance migrants realize higher survival rates at the cost of lower productivity because of reduced time on breeding areas relative to birds that migrate shorter distances and spend more time on breeding areas. RESULTS: Annual migration distances varied significantly among breeding areas (1020 to 12720 km), and were strongly negatively correlated with time spent on breeding areas (r = -0.986). Estimates of annual survival probability varied by wintering area (Pacific coast, Alaska Peninsula, and Eastern seaboard) and ranged from 0.79 (95%CI: 0.70-0.88) to 1.0, depending on criteria used to discern mortalities from radio failures. We did not find evidence for a linear relationship between migration distance and survival as swans from the breeding areas with the shortest and longest migration distances had the highest survival probabilities. Survival was lower in the first year post-marking than in subsequent years, but there was not support for seasonal differences in survival. Productivity varied among breeding populations and was generally inversely correlated to survival, but not migration distance or time spent on breeding areas. CONCLUSIONS: Tundra swans conformed to a major tenet of life history theory, as populations with the highest survival generally had the lowest productivity. The lack of a uniform relationship between time spent on breeding areas and productivity, or time spent on wintering areas and survival, indicates that factors other than temporal investment dictate demographic outcomes in this species. The tremendous diversity of migration strategies we identify in Alaskan tundra swans, without clear impacts on survival, underscores the ability of this species to adapt to different environments and climatic regimes.

Blood lead concentrations in Alaskan tundra swans: linking breeding and wintering areas with satellite telemetry.

Tundra swans (Cygnus columbianus) like many waterfowl species are susceptible to lead (Pb) poisoning, and Pb-induced mortality has been reported from many areas of their wintering range. Little is known however about Pb levels throughout the annual cycle of tundra swans, especially during summer when birds are on remote northern breeding areas where they are less likely to be exposed to anthropogenic sources of Pb. Our objective was to document summer Pb levels in tundra swans throughout their breeding range in Alaska to determine if there were population-specific differences in blood Pb concentrations that might pose a threat to swans and to humans that may consume them. We measured blood Pb concentrations in tundra swans at five locations in Alaska, representing birds that winter in both the Pacific Flyway and Atlantic Flyway. We also marked swans at each location with satellite transmitters and coded neck bands, to identify staging and wintering sites and determine if winter site use correlated with summer Pb concentrations. Blood Pb levels were generally low (<0.2 µg/ml) in swans across all breeding areas. Pb levels were lower in cygnets than adults, suggesting that swans were likely exposed to Pb on wintering areas or on return migration to Alaska, rather than on the summer breeding grounds. Blood Pb levels varied significantly across the five breeding areas, with highest concentrations in birds on the North Slope of Alaska (wintering in the Atlantic Flyway), and lowest in birds from the lower Alaska Peninsula that rarely migrate south for winter.

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.

Evidence that life history characteristics of wild birds influence infection and exposure to influenza A viruses.

We report on life history characteristics, temporal, and age-related effects influencing the frequency of occurrence of avian influenza (AI) viruses in four species of migratory geese breeding on the Yukon-Kuskokwim Delta, Alaska. Emperor geese (Chen canagica), cackling geese (Branta hutchinsii), greater white-fronted geese (Anser albifrons), and black brant (Branta bernicla), were all tested for active infection of AI viruses upon arrival in early May, during nesting in June, and while molting in July and August, 2006-2010 (n = 14,323). Additionally, prior exposure to AI viruses was assessed via prevalence of antibodies from sera samples collected during late summer in 2009 and 2010. Results suggest that geese are uncommonly infected by low pathogenic AI viruses while in Alaska. The percent of birds actively shedding AI viruses varied annually, and was highest in 2006 and 2010 (1-3%) and lowest in 2007, 2008, and 2009 (<0.70%). Contrary to findings in ducks, the highest incidence of infected birds was in late spring when birds first arrived from staging and wintering areas. Despite low prevalence, most geese were previously exposed to AI viruses, as indicated by high levels of seroprevalence during late summer (47%-96% across species; n = 541). Seroprevalence was >95% for emperor geese, a species that spends part of its life cycle in Asia and is endemic to Alaska and the Bering Sea region, compared to 40-60% for the other three species, whose entire life cycles are within the western hemisphere. Birds <45 days of age showed little past exposure to AI viruses, although antibodies were detected in samples from 5-week old birds in 2009. Seroprevalence of known age black brant revealed that no birds <4 years old had seroconverted, compared to 49% of birds ≥4 years of age.

Molecular detection of hematozoa infections in tundra swans relative to migration patterns and ecological conditions at breeding grounds.

Tundra swans (Cygnus columbianus) are broadly distributed in North America, use a wide variety of habitats, and exhibit diverse migration strategies. We investigated patterns of hematozoa infection in three populations of tundra swans that breed in Alaska using satellite tracking to infer host movement and molecular techniques to assess the prevalence and genetic diversity of parasites. We evaluated whether migratory patterns and environmental conditions at breeding areas explain the prevalence of blood parasites in migratory birds by contrasting the fit of competing models formulated in an occupancy modeling framework and calculating the detection probability of the top model using Akaike Information Criterion (AIC). We described genetic diversity of blood parasites in each population of swans by calculating the number of unique parasite haplotypes observed. Blood parasite infection was significantly different between populations of Alaska tundra swans, with the highest estimated prevalence occurring among birds occupying breeding areas with lower mean daily wind speeds and higher daily summer temperatures. Models including covariates of wind speed and temperature during summer months at breeding grounds better predicted hematozoa prevalence than those that included annual migration distance or duration. Genetic diversity of blood parasites in populations of tundra swans appeared to be relative to hematozoa prevalence. Our results suggest ecological conditions at breeding grounds may explain differences of hematozoa infection among populations of tundra swans that breed in Alaska.

Transmission and reassortment of avian influenza viruses at the Asian-North American interface.

Twenty avian influenza viruses were isolated from seven wild migratory bird species sampled at St. Lawrence Island, Alaska. We tested predictions based on previous phylogenetic analyses of avian influenza viruses that support spatially dependent trans-hemispheric gene flow and frequent interspecies transmission at a location situated at the Asian-North American interface. Through the application of phylogenetic and genotypic approaches, our data support functional dilution by distance of trans-hemispheric reassortants and interspecific virus transmission. Our study confirms infection of divergent avian taxa with nearly identical avian influenza strains in the wild. Findings also suggest that H16N3 viruses may contain gene segments with unique phylogenetic positions and that further investigation of how host specificity may impact transmission of H13 and H16 viruses is warranted.

Prevalence of Influenza A viruses in wild migratory birds in Alaska: patterns of variation in detection at a crossroads of intercontinental flyways.

BACKGROUND: The global spread of the highly pathogenic avian influenza H5N1 virus has stimulated interest in a better understanding of the mechanisms of H5N1 dispersal, including the potential role of migratory birds as carriers. Although wild birds have been found dead during H5N1 outbreaks, evidence suggests that others have survived natural infections, and recent studies have shown several species of ducks capable of surviving experimental inoculations of H5N1 and shedding virus. To investigate the possibility of migratory birds as a means of H5N1 dispersal into North America, we monitored for the virus in a surveillance program based on the risk that wild birds may carry the virus from Asia. RESULTS: Of 16,797 birds sampled in Alaska between May 2006 and March 2007, low pathogenic avian influenza viruses were detected in 1.7% by rRT-PCR but no highly pathogenic viruses were found. Our data suggest that prevalence varied among sampling locations, species (highest in waterfowl, lowest in passerines), ages (juveniles higher than adults), sexes (males higher than females), date (highest in autumn), and analytical technique (rRT-PCR prevalence = 1.7%; virus isolation prevalence = 1.5%). CONCLUSION: The prevalence of low pathogenic avian influenza viruses isolated from wild birds depends on biological, temporal, and geographical factors, as well as testing methods. Future studies should control for, or sample across, these sources of variation to allow direct comparison of prevalence rates.