Movements of wild ruddy shelducks in the Central Asian Flyway and their spatial relationship to outbreaks of highly pathogenic avian influenza H5N1

Abstract

Highly pathogenic avian influenza H5N1 remains a serious concern for both poultry and human health. Wild waterfowl are considered to be the reservoir for low pathogenic avian influenza viruses; however, relatively little is known about their movement ecology in regions where HPAI H5N1 outbreaks regularly occur. We studied movements of the ruddy shelduck (Tadorna ferruginea), a wild migratory waterfowl species that was infected in the 2005 Qinghai Lake outbreak. We defined their migration with Brownian Bridge utilization distribution models and their breeding and wintering grounds with fixed kernel home ranges. We correlated their movements with HPAI H5N1 outbreaks, poultry density, land cover, and latitude in the Central Asian Flyway. Our Akaike Information Criterion analysis indicated that outbreaks were correlated with land cover, latitude, and poultry density. Although shelduck movements were included in the top two models, they were not a top parameter selected in AICc stepwise regression results. However, timing of outbreaks suggested that outbreaks in the flyway began during the winter in poultry with spillover to wild birds during the spring migration. Thus, studies of the movement ecology of wild birds in areas with persistent HPAI H5N1 outbreaks may contribute to understanding their role in transmission of this disease.

Figure 1

General movement patterns for 26 ruddy shelducks marked with satellite transmitters at Qinghai Lake, China. Study area and movement paths (red lines) for 26 ruddy shelducks marked with satellite transmitters in 2007–2008 and tracked through 15 May 2010. White polygons represent Minimum Convex Polygons (MCP) encompassing locations at breeding, wintering and stop-over areas.

Figure 2

Seasonal movements (fall migration, winter, spring migration, and breeding/post-breeding) over three years for ruddy shelducks marked at Qinghai Lake, China. Seasonal movements were calculated for 20 shelducks with at least one full fall migration; birds with multiple annual cycles were treated as unique individuals in subsequent years. Light gray bars give median period start dates to median end dates, dark gray depicts the innermost 75th percentile, and error bars indicate first and last recorded dates within a period.

Figure 3

Utilization distributions for ruddy shelducks marked at Qinghai Lake, China, 2007–2008; shown in relation to poultry density (brown shading) and HP H5N1 outbreaks, occurring in wild birds (white circles) and poultry (black circles), from September 2003 to April 2010. Brownian bridge utilization distributions describe (A) spring (10 March–4 May) and (C) fall (27 October–20 December) migration movements. Fixed kernel home ranges depict population level (B) breeding (5 May–26 October) and (D) wintering (21 December–9 March) areas. Two shading levels (red, purple) for all utilization distributions indicate isopleths containing 95% and 99% of total locations, respectively.

Figure 4

Routes for ruddy shelducks marked at Qinghai Lake, China and followed for at least two seasonal migratory cycles. Repeated migratory routes for seven ruddy shelducks marked at Qinghai Lake, 2007–2008. All seven shelducks completed two or more full migration movements (fall and spring). Paths are given for (A) fall (2007–2009) and (B) spring (2008–2010) migration movements, with solid, dashed, and dotted lines as first, second, and third journeys, respectively.

Figure 5

Comparison of wild and domestic outbreaks from 2003–2010 by seasonal period in the life cycle of ruddy shelducks. Observed vs. expected values differed for both (A) wild bird and (B) domestic poultry outbreaks when tested separately (wild: P = 0.043, Fisher Exact Test; poultry: P < 0.0001, Chi-Squared Test). Expected numbers were calculated under the assumption that outbreaks are proportional to the number of days within the fixed seasonal period (fall migration = 55 d; winter = 79 d; spring migration = 56 d; and breeding = 175 d).

Figure 6

Correlation and regression tree for wild bird and domestic poultry outbreaks in the Central Asian Flyway. Expected numbers were calculated assuming outbreaks were proportional to seasonal period length. Values in circles indicate the variable and if differences were significant, while numbers along the tree branches indicate separation points for that variable in order of highest importance from top-to-bottom.