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Lessons learned from research and surveillance directed at highly pathogenic influenza A viruses in wild birds inhabiting North America

Following detections of highly pathogenic (HP) influenza A viruses (IAVs) in wild birds inhabiting East Asia after the turn of the millennium, the intensity of sampling of wild birds for IAVs increased throughout much of North America. The objectives for many research and surveillance efforts were directed towards detecting Eurasian origin HP IAVs and understanding the potential of such viruses to be maintained and dispersed by wild birds. In this review, we highlight five important lessons learned from research and surveillance directed at HP IAVs in wild birds inhabiting North America: (1) Wild birds may disperse IAVs between North America and adjacent regions via migration, (2) HP IAVs can be introduced to wild birds in North America, (3) HP IAVs may cross the wild bird-poultry interface in North America, (4) The probability of encountering and detecting a specific virus may be low, and (5) Population immunity of wild birds may influence HP IAV outbreaks in North America. We review empirical support derived from research and surveillance efforts for each lesson learned and, furthermore, identify implications for future surveillance efforts, biosecurity, and population health. We conclude our review by identifying five additional areas in which we think future mechanistic research relative to IAVs in wild birds in North America are likely to lead to other important lessons learned in the years ahead.

Virology

Variation in migratory behavior influences regional genetic diversity and structure among American kestrel populations (Falco sparverius) in North America

Birds employ numerous strategies to cope with seasonal fluctuations in high-quality habitat availability. Long distance migration is a common tactic; however, partial migration is especially common among broadly distributed species. Under partial migration systems, a portion of a species migrates, whereas the remainder inhabits breeding grounds year round. In this study, we identified effects of migratory behavior variation on genetic structure and diversity of American Kestrels (Falco sparverius), a widespread partial migrant in North America. American Kestrels generally migrate; however, a resident group inhabits the southeastern United States year round. The southeastern group is designated as a separate subspecies (F. s. paulus) from the migratory group (F. s. sparverius). Using mitochondrial DNA and microsatellites from 183 and 211 individuals, respectively, we illustrate that genetic structure is stronger among nonmigratory populations, with differentiation measures ranging from 0.060 to 0.189 depending on genetic marker and analysis approach. In contrast, measures from western North American populations ranged from 0 to 0.032. These findings suggest that seasonal migratory behavior is also associated with natal and breeding dispersal tendencies. We likewise detected significantly lower genetic diversity within nonmigratory populations, reflecting the greater influence of genetic drift in small populations. We identified the signal of population expansion among nonmigratory populations, consistent with the recent establishment of higher latitude breeding locations following Pleistocene glacial retreat. Differentiation of F. s. paulus and F. s. sparverius reflected subtle differences in allele frequencies. Because migratory behavior can evolve quickly, our analyses suggest recent origins of migratory American Kestrel populations in North America.

Journal of Heredity

Roost- and perch-site selection by Golden Eagles (Aquila chrysaetos) in eastern North America

Birds select critical resources to meet needs that vary in response to spatial, temporal, and individual variation. As an example, perch or roost sites may be at locations that provide protection from predators, mobbing, or inclement weather. Applied to large, soaring predators, this theory suggests that they may select perch and roost sites near food resources or at sites where environmental updrafts develop. To test these theories, we characterized selection of nonflight locations throughout the annual cycle for Golden Eagles ( Aquila chrysaetos ) in eastern North America. We determined factors associated with selection of perching (daytime) and roosting (nighttime) sites by eagles by comparing land cover and topographic characteristics of GPS telemetry locations for eagles (used) with random (available) locations. We separately assessed selection for perch and roost sites during each of 4 seasons (winter, summer, and spring and fall migration). Golden Eagles showed different selection patterns for perching by season and age. Throughout the year, eagles selected perch sites on steep slopes. The direction these slopes faced differed among seasons, with eagles selecting south-facing slopes in summer and east-facing slopes during migration. Adults showed greater preferences for broadleaf forests in summer and for ridges in fall. Patterns of perch-site use were consistent with selection for sites that provide thermal protection and access to thermal updrafts. We found few patterns of selection for roosting sites. Our analysis provides insight into decision-making by a longdistance migrant across its annual cycle and throughout its geographic range, and thus into how resource selection changes seasonally.

Wilson Journal of Ornithology

Large-scale studies of marked birds in North America

The first large-scale, co-operative, studies of marked birds in North America were attempted in the 1950s. Operation Recovery, which linked numerous ringing stations along the east coast in a study of autumn migration of passerines, and the Preseason Duck Ringing Programme in prairie states and provinces, conclusively demonstrated the feasibility of large-scale projects. The subsequent development of powerful analytical models and computing capabilities expanded the quantitative potential for further large-scale projects. Monitoring Avian Productivity and Survivorship, and Adaptive Harvest Management are current examples of truly large-scale programmes. Their exemplary success and the availability of versatile analytical tools are driving changes in the North American bird ringing programme. Both the US and Canadian ringing offices are modifying operations to collect more and better data to facilitate large-scale studies and promote a more project-oriented ringing programme. New large-scale programmes such as the Cornell Nest Box Network are on the horizon.

Bird Study

Highly pathogenic avian influenza is an emerging disease threat to wild birds in North America

Prior to the emergence of the A/goose/Guangdong/1/1996 (Gs/GD) H5N1 influenza A virus, the long-held and well-supported paradigm was that highly pathogenic avian influenza (HPAI) outbreaks were restricted to poultry, the result of cross-species transmission of precursor viruses from wild aquatic birds that subsequently gained pathogenicity in domestic birds. Therefore, management agencies typically adopted a prevention, control, and eradication strategy that included strict biosecurity for domestic bird production, isolation of infected and exposed flocks, and prompt depopulation. In most cases, this strategy has proved sufficient for eradicating HPAI. Since 2002, this paradigm has been challenged with many detections of viral descendants of the Gs/GD lineage among wild birds, most of which have been associated with sporadic mortality events. Since the emergence and evolution of the genetically distinct clade 2.3.4.4 Gs/GD lineage HPAI viruses in approximately 2010, there have been further increases in the occurrence of HPAI in wild birds and geographic spread through migratory bird movement. A prominent example is the introduction of clade 2.3.4.4 Gs/GD HPAI viruses from East Asia to North America via migratory birds in autumn 2014 that ultimately led to the largest outbreak of HPAI in the history of the United States. Given the apparent maintenance of Gs/GD lineage HPAI viruses in a global avian reservoir; bidirectional virus exchange between wild and domestic birds facilitating the continued adaptation of Gs/GD HPAI viruses in wild bird hosts; the current frequency of HPAI outbreaks in wild birds globally, and particularly in Eurasia where Gs/GD HPAI viruses may now be enzootic; and ongoing dispersal of AI viruses from East Asia to North America via migratory birds, HPAI now represents an emerging disease threat to North American wildlife. This recent paradigm shift implies that management of HPAI in domestic birds alone may no longer be sufficient to eradicate HPAI viruses from a given country or region. Rather, agencies managing wild birds and their habitats may consider the development or adoption of mitigation strategies to minimize introductions to poultry, to reduce negative impacts on wild bird populations, and to diminish adverse effects to stakeholders using wildlife resources. The main objective of this review is, therefore, to provide information that will assist wildlife managers in developing mitigation strategies or approaches for dealing with outbreaks of Gs/GD HPAI in wild birds in the form of preparedness, surveillance, research, communications, and targeted management actions. Resultant outbreak response plans and actions may represent meaningful steps of wildlife managers toward the use of collaborative and multi-jurisdictional One Health approaches when it comes to the detection, investigation, and mitigation of emerging viruses at the human-domestic animal-wildlife interface.

Journal of Wildlife Management

Pasteurella multocida isolated from wild birds of North America: a serotype and DNA fingerprint study of isolates from 1978 to 1993

Serotype and DNA fingerprint methods were used to study Pasteurella multocida isolated from 320 wild birds of North America. Isolates were collected during 1978-93. The HhaI profiles of 314 isolates matched the HhaI profile of somatic reference type 1, strain X-73; somatic type 1 antigen was expressed by 310 isolates, and the serotype of four isolates was undetected. Differentiation of the 314 isolates was observed by digestion of DNA with HpaII. None of the HpaII profiles matched the HpaII profile of X-73 (designated HhaI 001/HpaII 001). Three HpaII profiles were recognized among the somatic type 1 isolates: HpaII 002 (n = 18), HpaII 003 (n = 122), and HpaII 004 (n = 174). Profile HpaII 002 was found among isolates collected during 1979-83. Profile HpaII 003 was identified from isolates collected during 1979-89, with the exception of two isolates in 1992. The HpaII 004 profile was identified from isolates collected during 1983-93. Of the six remaining isolates, four expressed somatic type 4 and had HhaI profiles identical to the somatic type 4 reference strain P-1662 profile (designated HhaI 004); these isolates were differentiated by digestion of DNA with HpaII. One isolate was identified as serotype F:11, and another was serotype A:3,4. In the present study, 314 of 316 (99.4%) isolates from wild birds in the Central, Mississippi, and Pacific flyways during 1978-93, were P. multocida somatic type 1.

Avian Diseases

Application of models to conservation planning for terrestrial birds in North America

Partners in Flight (PIF), a public–private coalition for the conservation of land birds, has developed one of four international bird conservation plans recognized under the auspices of the North American Bird Conservation Initiative (NABCI). Partners in Flight prioritized species most in need of conservation attention and set range-wide population goals for 448 species of terrestrial birds. Partnerships are now tasked with developing spatially explicit estimates of the distribution, and abundance of priority species across large ecoregions and identifying habitat acreages needed to support populations at prescribed levels. The PIF Five Elements process of conservation design identifies five steps needed to implement all bird conservation at the ecoregional scale. Habitat assessment and landscape characterization describe the current amounts of different habitat types and summarize patch characteristics, and landscape configurations that define the ability of a landscape to sustain healthy bird populations and are a valuable first step to describing the planning area before pursuing more complex species-specific models. Spatially linked database models, landscape-scale habitat suitability models, and statistical models are viable alternatives for predicting habitat suitability or bird abundance across large planning areas to help assess conservation opportunities, design landscapes to meet population objectives, and monitor change in habitat suitability or bird numbers over time. Bird conservation in the United States is a good example of the use of models in large-scale wildlife conservation planning because of its geographic extent, focus on multiple species, involvement of multiple partners, and use of simple to complex models. We provide some background on the recent development of bird conservation initiatives in the United States and the approaches used for regional conservation assessment and planning. We focus on approaches being used for landscape characterization and assessment, and bird population response modeling.

Book chapter

Genetic evidence supports sporadic and independent introductions of subtype H5 low pathogenic avian influenza A viruses from wild birds to domestic poultry in North America

Wild bird–origin influenza A viruses (IAVs or avian influenza) have led to sporadic outbreaks among domestic poultry in the United States (US) and Canada, resulting in economic losses through the implementation of costly containment practices and destruction of birds. We used evolutionary analyses of virus sequence data to determine that 78 H5 low pathogenic avian influenza viruses (LPAIVs) isolated from domestic poultry in the US and Canada during 2001–2017 resulted from 18 independent virus introductions from wild birds. Within the wild bird reservoir, the hemagglutinin gene segments of H5 LPAIVs exist primarily as two co-circulating genetic sublineages, and our findings suggest the H5 gene segments flow within each migratory bird flyway and among adjacent flyways, with limited exchange between the non-adjacent Atlantic and Pacific Flyways. Phylogeographic analyses provided evidence that IAVs from dabbling ducks and swans/geese contributed to emergence of viruses among domestic poultry. H5 LPAIVs isolated from commercial farm poultry (i.e. turkey) were descended from a single introduction typically remain a single genotype, whereas those from live bird markets sometimes led to multiple genotypes, reflecting the potential for reassortment with other IAVs circulating within live bird markets. H5 LPAIV introduced from wild birds to domestic poultry represent economic threats to the U.S. poultry industry, and our data suggest that such introductions have been sporadic, controlled effectively through production monitoring and a stamping-out policy, and are, therefore, unlikely to result in sustained detections in commercial poultry operations.

Journal of Virology

Rapid expansion of genotype D1.1 A(H5N1) influenza viruses in wild birds across North America during the 2024 migratory season

In late 2021, high pathogenicity avian influenza A(H5N1) clade 2.3.4.4b viruses entered North America and reassorted rapidly with local avian influenza viruses. In September 2024, we detected a new reassortant later classified as genotype D1.1. Using active and passive avian influenza surveillance across Canada and the USA, we tracked the emergence and rapid spread of D1.1 viruses in wild birds during the 2024 fall migration. Phylodynamic analysis showed that D1.1 viruses formed a monophyletic group and displaced earlier A(H5) genotypes across several flyways. Their expansion coincided with detections in other hosts, including 17 human cases, 4 of which were severe or fatal. None of the mammalian-adaptive markers detected in human cases were found in wild bird viruses, and candidate vaccine viruses retained antigenic cross-reactivity with D1.1 strains.

Nature medicine

Techniques and results of nongame bird monitoring in North America

Long-term bird population trends based on accumulated ratios (proportional change) sometimes give a very misleading view of population change. Alternate methods of representing population change, based on the weighted means for the individual years, avoid the dangers of using ratios. Some advantages and disadvantages of various weighting techniques are discussed.

Book chapter