Hampered foraging and migratory performance in swans infected with low-pathogenic avian influenza A virus

Abstract

It is increasingly acknowledged that migratory birds, notably waterfowl, play a critical role in the maintenance and spread of influenza A viruses. In order to elucidate the epidemiology of influenza A viruses in their natural hosts, a better understanding of the pathological effects in these hosts is required. Here we report on the feeding and migratory performance of wild migratory Bewick's swans (Cygnus columbianus bewickii Yarrell) naturally infected with low-pathogenic avian influenza (LPAI) A viruses of subtypes H6N2 and H6N8. Using information on geolocation data collected from Global Positioning Systems fitted to neck-collars, we show that infected swans experienced delayed migration, leaving their wintering site more than a month after uninfected animals. This was correlated with infected birds travelling shorter distances and fuelling and feeding at reduced rates. The data suggest that LPAI virus infections in wild migratory birds may have higher clinical and ecological impacts than previously recognised.

Figure 1

Bewick's swan 923A infected with an H6 influenza A virus. This (adult) individual not only carried an active influenza infection, it also showed the highest antibody response among all 25 sampled birds. Photo by W. Tijsen.

Figure 2

Phylogenetic tree for H6 influenza A viruses isolated from swans. The DNA maximum likelihood tree was constructed using A/pintail/Alberta/210/2002 (H1N1) as out-group and includes sequences from public databases. Genes clustered into four different groups as described by Spackman et al. . The scale bar represents ∼10% of nucleotide changes between close relatives. Small numbers in the tree represent the bootstrap values.

Figure 3

Timing of migration in healthy and infected swans. (A) Infected swans left the study area more than a month after the uninfected birds, indicated by broad vertical grey bars ranging from mean-SE to mean+SE. Moreover, their mean net displacement after departure (closed dots±dashed SE-lines) was shorter than for the uninfected birds (open dots±dashed SE-lines). Sample sizes of displacements estimates: n = 2 for infected birds (whole time span); sample size declined for uninfected birds due to birds that flew out of range: n = 10 (days 0–41), n = 9 (42–47), and n = 8 (48–55). (B) Total number of swans in our study area declined more or less gradually over time (W. Tijsen et al. unpubl. data), suggesting a continuous departure of about 30 birds per day (apart from the short dip around day 12 during a snowy cold spell).

Figure 4

Feeding parameters as a function of health status. Compared to healthy birds, infected birds (A) fuelled slower, (B) took fewer bites per hour, and (C) took fewer bites per produced dropping. Because of a seasonal increase observed in bite rate (p<0.05 when all observations pooled), bite rate plotted in (B) were standardized to 1 February. In all graphs, bars give least-square means, error bars are SE.