Dirk V. Derksen

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

BackgroundThe 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.ResultsOf 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%).ConclusionThe 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.

NATAL AND BREEDING PHILOPATRY IN A BLACK BRANT, BRANTA BERNICLA NIGRICANS, METAPOPULATION

We estimated natal and breeding philopatry and dispersal probabilities for a metapopulation of Black Brant (Branta bernicla nigricans) based on observations of marked birds at six breeding colonies in Alaska, 1986–1994. Both adult females and males exhibited high (>0.90) probability of philopatry to breeding colonies. Probability of natal philopatry was significantly higher for females than males. Natal dispersal of males was recorded between every pair of colonies, whereas natal dispersal of females was observed between only half of the colony pairs. We suggest that female-biased philopatry was the result of timing of pair formation and characteristics of the mating system of brant, rather than factors related to inbreeding avoidance or optimal discrepancy. Probability of natal philopatry of females increased with age but declined with year of banding. Age-related increase in natal philopatry was positively related to higher breeding probability of older females. Declines in natal philopatry with year of banding corresponded negatively to a period of increasing population density; therefore, local population density may influence the probability of nonbreeding and gene flow among colonies.

Avian influenza at both ends of a migratory flyway: characterizing viral genomic diversity to optimize surveillance plans for North America

Although continental populations of avian influenza viruses are genetically distinct, transcontinental reassortment in low pathogenic avian influenza (LPAI) viruses has been detected in migratory birds. Thus, genomic analyses of LPAI viruses could serve as an approach to prioritize species and regions targeted by North American surveillance activities for foreign origin highly pathogenic avian influenza (HPAI). To assess the applicability of this approach, we conducted a phylogenetic and population genetic analysis of 68 viral genomes isolated from the northern pintail (Anas acuta) at opposite ends of the Pacific migratory flyway in North America. We found limited evidence for Asian LPAI lineages on wintering areas used by northern pintails in California in contrast to a higher frequency on breeding locales of Alaska. Our results indicate that the number of Asian LPAI lineages observed in Alaskan northern pintails, and the nucleotide composition of LPAI lineages, is not maintained through fall migration. Accordingly, our data indicate that surveillance of Pacific Flyway northern pintails to detect foreign avian influenza viruses would be most effective in Alaska. North American surveillance plans could be optimized through an analysis of LPAI genomics from species that demonstrate evolutionary linkages with European or Asian lineages and in regions that have overlapping migratory flyways with areas of HPAI outbreaks.

Intercontinental reassortment and genomic variation of low pathogenic avian influenza viruses isolated from northern pintails ( Anas acuta ) in Alaska: examining the evidence through space and time

Migration and population genetic data for northern pintails (Anas acuta) and phylogenetic analysis of low pathogenic avian influenza (LPAI) viruses from this host in Alaska suggest that northern pintails are involved in ongoing intercontinental transmission of avian influenza. Here, we further refine this conclusion through phylogenetic analyses which demonstrate that detection of foreign lineage gene segments is spatially dependent and consistent through time. Our results show detection of foreign lineage gene segments to be most likely at sample locations on the Alaska Peninsula and least likely along the Southern Alaska Coast. Asian lineages detected at four gene segments persisted across years, suggesting maintenance in avian hosts that migrate to Alaska each year from Asia or in hosts that remain in Alaska throughout the year. Alternatively, live viruses may persist in the environment and re-infect birds in subsequent seasons.

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.

PHYLOGEOGRAPHY OF CANADA GEESE (BRANTA CANADENSIS) IN WESTERN NORTH AMERICA

Abstract Using molecular genetic markers that differ in mode of inheritance and rate of evolution, we examined levels and partitioning of genetic variation for seven nominal subspecies (11 breeding populations) of Canada Geese (Branta canadensis) in western North America. Gene trees constructed from mtDNA control region sequence data show that subspecies of Canada Geese do not have distinct mtDNA. Large and small-bodied forms of Canada Geese were highly diverged (0.077 average sequence divergence) and represent monophyletic groups. A majority (65%) of 20 haplotypes resolved were observed in single breeding locales. However, within both large and small-bodied forms certain haplotypes occurred across multiple subspecies. Population trees for both nuclear (microsatellites) and mitochondrial markers were generally concordant and provide resolution of population and subspecific relationships indicating incomplete lineage sorting. All populations and subspecies were genetically diverged, but to varying degrees. Analyses of molecular variance, nested-clade and coalescencebased analyses of mtDNA suggest that both historical (past fragmentation) and contemporary forces have been important in shaping current spatial genetic distributions. Gene flow appears to be ongoing though at different rates, even among currently recognized subspecies. The efficacy of current subspecific taxonomy is discussed in light of hypothesized historical vicariance and current demographic trends of management and conservation concern.

Response of fall-staging brant and Canada geese to aircraft overflights in southwestern Alaska

Because much of the information concerning disturbance of waterfowl by aircraft is anecdotal we examined behavioral responses of Pacific brant (Brauta beruicla nigricans) and Canada geese (B. canadensis taverneri) to experimental overflights during fall stagmg at Izembek Lagoon, Alaska. These data were used to develop predictive models of brant and Canada goose response to aircraft altitude, type, noise, and lateral distance from flocks. Overall, 75% of brant flocks and 9% of Canada goose flocks flew in response to overflights. Mean flight and alert responses of both species were greater for rotary-wing than for fixed-wing aircraft and for high-noise than for low-noise aircraft. Increased lateral distance between an aircraft and a flock was the most consistent predictive parameter associated with lower probability of a response by geese. Altitude was a less reliable predictor because of interaction effects with aircraft type and noise. Although mean respouse of brant and Canada geese nerally was inversely proportional to aireraft altitude, reatest respouse occurred at intermediate (305-760 m) altitudes. At Izembek Lagoon and other areas where there are large concentrations of waterfowl, managers should consider lateral distance from the birds as the primary criterion for establishing local flight restrictions, especially for helicopters.

Breeding-Season Sympatry Facilitates Genetic Exchange Among Allopatric Wintering Populations of Northern Pintails in Japan and California

Abstract. The global redistribution of pathogens, such as highly pathogenic avian influenza, has renewed interest in the connectivity of continental populations of birds. Populations of the Northern Pintail (Anas acuta) wintering in Japan and California are considered separate from a management perspective. We used data from band recoveries and population genetics to assess the degree of biological independence of these wintering populations. Distributions of recoveries in Russia of Northern Pintails originally banded during winter in North America overlapped with distributions of Northern Pintails banded during winter in Japan. Thus these allopatric wintering populations are partially sympatric during the breeding season. The primary areas of overlap were along the Chukotka and Kamchatka peninsulas in Russia. Furthermore, band recoveries demonstrated dispersal of individuals between wintering populations both from North America to Japan and vice versa. Genetic analyses of samples from both wintering populations showed little evidence of population differentiation. The combination of banding and genetic markers demonstrates that these two continental populations are linked by low levels of dispersal as well as likely interbreeding in eastern Russia. Although the levels of dispersal are inconsequential for population dynamics, the combination of dispersal and interbreeding represents a viable pathway for exchange of genes, diseases, and/or parasites.

A genetic evaluation of morphology used to identify harvested Canada geese

Using maximum likelihood estimators (in genetic stock identification), we used genetic markers to evaluate the utility of 2 morphological measures (culmen length and plumage color) to correctly identify groups of hunter-harvested dusky (Branta canadensis occidentalis) and dusky-like Canada geese on the wintering grounds within the Pacific Flyway. Significant levels of genetic differentiation were observed across all sampled breeding sites for both nuclear microsatellite loci and mtDNA when analyzed at the sequence level. The ability to discriminate among geese from these sites using genetic markers was further demonstrated using computer simulations. We estimated contributions from the Copper River Delta, the primary breeding area of dusky Canada geese, to groups of hunter-harvested geese classified as dusky Canada geese on the basis of morphology as 50.6 ± 10.1(SE)% for females and 50.3 ± 13.0% for males. We also estimated that 16 ± 8.1% of females classified as dusky Canada geese on the basis of morphology originated from Middleton Island, Alaska; a locale currently managed as a subpopulation of dusky Canada geese, even though the majority of geese from this area possess a unique mtDNA haplotype not found on the Copper River Delta. The use of culmen length and plumage color to identify the origin of breeding populations in the harvest provides conservative criteria for management of dusky Canada geese as individuals of other breeding populations are misassigned as dusky Canada geese and birds of the lighter-plumaged dusky-like group did not appear to originate from breeding sites of the dusky Canada goose. Our analyses demonstrate that genetic markers can accurately estimate the proportion of genetically differentiated areas that comprise an admixed group, but they also raise questions about the management scale of Pacific Flyway Canada geese (e.g., at the subspecies or breeding population level) and the use of morphological and genetic characteristics to monitor the harvest of different populations within admixed wintering flocks.

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.