Pathways for avian influenza virus spread: GPS reveals wild waterfowl in commercial livestock facilities and connectivity with the natural wetland landscape

McDuie, Fiona; Matchett, Elliott L.; Prosser, Diann J.; Takekawa, John Y.; Pitesky, Maurice; Lorenz, Austen A.; McCuen, Madeline M.; Overton, Cory T.; Ackerman, Joshua T.; Cruz, Susan E. W. De La; Casazza, Michael L.

doi:10.1111/tbed.14445

Cited by 21 publications

(8 citation statements)

References 102 publications

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“…The Central Valley and San Francisco Bay Estuary of California are hotspots of mercury contamination in North America [4,46] and are important sites for overwintering waterfowl; approximately 60% of the migratory waterfowl in the Pacific Flyway overwinter in this region annually [47,48]. Multiple waterfowl species co-occur at overwintering sites in the region, which enables cross-species influenza transmission and viral reassortment [49,50], and waterfowl occasionally use wetlands and agricultural habitats near and within poultry facilities [51]. This combination of mercury contamination, high waterfowl abundance and intensive poultry production makes northern California an important region for understanding how mercury contamination affects influenza prevalence and wildlife health.…”

Section: Introductionmentioning

confidence: 99%

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl

et al. 2022

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Environmental contamination is widespread and can negatively impact wildlife health. Some contaminants, including heavy metals, have immunosuppressive effects, but prior studies have rarely measured contamination and disease simultaneously, which limits our understanding of how contaminants and pathogens interact to influence wildlife health. Here, we measured mercury concentrations, influenza infection, influenza antibodies and body condition in 749 individuals from 11 species of wild ducks overwintering in California. We found that the odds of prior influenza infection increased more than fivefold across the observed range of blood mercury concentrations, while accounting for species, age, sex and date. Influenza infection prevalence was also higher in species with higher average mercury concentrations. We detected no relationship between influenza infection and body fat content. This positive relationship between influenza prevalence and mercury concentrations in migratory waterfowl suggests that immunotoxic effects of mercury contamination could promote the spread of avian influenza along migratory flyways, especially if influenza has minimal effects on bird health and mobility. More generally, these results show that the effects of environmental contamination could extend beyond the geographical area of contamination itself by altering the prevalence of infectious diseases in highly mobile hosts.

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Section: Introductionmentioning

confidence: 99%

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl

et al. 2022

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“…Previous studies mostly tried to explain the variation in the occurrence of HPAIV introductions with environmental variables, such as distance to waterways and vegetation index [ 18 , 19 , 33 ]. Others also included surveillance or telemetry data to track the movements of a selection of wild bird species in a certain time period [ 17 , 29 , 32 , 34 , 35 , 36 ], but most studies did not include detailed count data on wild bird species distribution to analyze HPAIV introductions on poultry farms. Environmental variables can be considered as a proxy for habitat suitability for wild birds, and were, in our study, less suitable predictors than the densities of the actual bird species.…”

Section: Discussionmentioning

confidence: 99%

“…Such data have proven valuable in many previous spatiotemporal analyses. For example, it has been shown in many studies that the presence of wetlands is vital as they are an important habitat for many waterfowl species [ 32 , 33 , 35 ]. In the current study, the original land cover classes were aggregated into five major classes, which decreased the resolution of land cover classification in the analyses, and may have reduced sensitivity of these variables for the prediction of farm outbreak probability.…”

Section: Discussionmentioning

confidence: 99%

Wild Bird Densities and Landscape Variables Predict Spatial Patterns in HPAI Outbreak Risk across The Netherlands

et al. 2022

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Highly pathogenic avian influenza viruses’ (HPAIVs) transmission from wild birds to poultry occurs globally, threatening animal and public health. To predict the HPAI outbreak risk in relation to wild bird densities and land cover variables, we performed a case-control study of 26 HPAI outbreaks (cases) on Dutch poultry farms, each matched with four comparable controls. We trained machine learning classifiers to predict outbreak risk with predictors analyzed at different spatial scales. Of the 20 best explaining predictors, 17 consisted of densities of water-associated bird species, 2 of birds of prey, and 1 represented the surrounding landscape, i.e., agricultural cover. The spatial distribution of mallard (Anas platyrhynchos) contributed most to risk prediction, followed by mute swan (Cygnus olor), common kestrel (Falco tinnunculus) and brant goose (Branta bernicla). The model successfully distinguished cases from controls, with an area under the receiver operating characteristic curve of 0.92, indicating accurate prediction of HPAI outbreak risk despite the limited numbers of cases. Different classification algorithms led to similar predictions, demonstrating robustness of the risk maps. These analyses and risk maps facilitate insights into the role of wild bird species and support prioritization of areas for surveillance, biosecurity measures and establishments of new poultry farms to reduce HPAI outbreak risks.

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“…Capture timing, locations, and techniques varied by species and included funnel traps, rocket/cannon nets, swim‐in corrals, and handheld dip nets. For more details on capture and marking, see Appendix S1: Supplementary Methods and Figure S1, McDuie, Casazza, Overton, et al (2019), and McDuie et al (2022). Pintails were captured in September, October, and February 2016–2019 in and near Suisun Marsh (San Francisco Bay Estuary; 38.138, −121.978), Colusa National Wildlife Refuge (NWR; 39.145, −122.044), and the Upper Butte Basin Wildlife Area (WA) in the Central Valley (39.467, −121.877).…”

Section: Methodsmentioning

confidence: 99%

Waterfowl recently infected with low pathogenic avian influenza exhibit reduced local movement and delayed migration

et al. 2023

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Understanding relationships between infection and wildlife movement patterns is important for predicting pathogen spread, especially for multispecies pathogens and those that can spread to humans and domestic animals, such as avian influenza viruses (AIVs). Although infection with low pathogenic AIVs is generally considered asymptomatic in wild birds, prior work has shown that influenza‐infected birds occasionally delay migration and/or reduce local movements relative to their uninfected counterparts. However, most observational research to date has focused on a few species in northern Europe; given that influenza viruses are widespread globally and outbreaks of highly pathogenic strains are increasingly common, it is important to explore influenza–movement relationships across more species and regions. Here, we used telemetry data to investigate relationships between influenza infection and movement behavior in 165 individuals from four species of North American waterfowl that overwinter in California, USA. We studied both large‐scale migratory and local overwintering movements and found that relationships between influenza infection and movement patterns varied among species. Northern pintails (Anas acuta) with antibodies to avian influenza, indicating prior infection, made migratory stopovers that averaged 12 days longer than those with no influenza antibodies. In contrast, greater white‐fronted geese (Anser albifrons) with antibodies to avian influenza made migratory stopovers that averaged 15 days shorter than those with no antibodies. Canvasbacks (Aythya valisineria) that were actively infected with influenza upon capture in the winter delayed spring migration by an average of 28 days relative to birds that were uninfected at the time of capture. At the local scale, northern pintails and canvasbacks that were actively infected with influenza used areas that were 7.6 and 4.9 times smaller than those of uninfected ducks, respectively, during the period of presumed active influenza infection. We found no evidence for an influence of active influenza infection on local movements of mallards (Anas platyrhynchos). These results suggest that avian influenza can influence waterfowl movements and illustrate that the relationships between avian influenza infection and wild bird movements are context‐ and species‐dependent. More generally, understanding and predicting the spread of multihost pathogens requires studying multiple taxa across space and time.

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Pathways for avian influenza virus spread: GPS reveals wild waterfowl in commercial livestock facilities and connectivity with the natural wetland landscape

Cited by 21 publications

References 102 publications

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl

Wild Bird Densities and Landscape Variables Predict Spatial Patterns in HPAI Outbreak Risk across The Netherlands

Waterfowl recently infected with low pathogenic avian influenza exhibit reduced local movement and delayed migration

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