Long-term variation in influenza A virus prevalence and subtype diversity in migratory mallards in northern Europe

Abstract

Data on long-term circulation of pathogens in wildlife populations are seldom collected, and hence understanding of spatial-temporal variation in prevalence and genotypes is limited. Here, we analysed a long-term surveillance series on influenza A virus (IAV) in mallards collected at an important migratory stopover site from 2002 to 2010, and characterized seasonal dynamics in virus prevalence and subtype diversity. Prevalence dynamics were influenced by year, but retained a common pattern for all years whereby prevalence was low in spring and summer, but increased in early autumn with a first peak in August, and a second more pronounced peak during October-November. A total of 74 haemagglutinin (HA)/neuraminidase (NA) combinations were isolated, including all NA and most HA (H1-H12) subtypes. The most common subtype combinations were H4N6, H1N1, H2N3, H5N2, H6N2 and H11N9, and showed a clear linkage between specific HA and NA subtypes. Furthermore, there was a temporal structuring of subtypes within seasons based on HA phylogenetic relatedness. Dissimilar HA subtypes tended to have different temporal occurrence within seasons, where the subtypes that dominated in early autumn were rare in late autumn, and vice versa. This suggests that build-up of herd immunity affected IAV dynamics in this system.

Keywords: disease dynamics; diversity; host–pathogen interactions; influenza A virus; mallards; prevalence.

Figure 1.

Seasonal variation in (a) trapping of mallards and (b) IAV prevalence 2002–2010. In (a) the y-axis depicts the average number of newly trapped birds, and data are presented as bar plots with error bars. The secondary y-axis shows the variation of newly trapped birds compared with total for all years with 95% CI. The circles show the raw estimates for influx computed on data pooled across years, stratified by week. In (b), the y-axis gives the seasonal variation in prevalence, where the raw estimates of prevalence are given by filled circles, and the continuous line represents the estimated prevalence by the spline model, and the discontinuous lines the 95% CI. In both panels, the x-axis depicts the annual time scale in weeks.

Figure 2.

Temporal diversity of HA and NA (years 2002–2009). Filled boxes show the number of virus isolates within a two week period, where a topographic colour scale was used to indicate subtype abundance, with increasing numbers of isolates depicted as green and blue in the scale. The y-axis indicates the subtypes, the dendrogram shows subtype phylogenetic relatedness and thicker coloured branches indicate the HA classes. The H1 class is represented in red, the H3 class in black and the H11 class in green. Long periods of time without retrieved isolates were not included and are indicated with diagonal lines on the temporal x-axis to indicate discontinuous time.

Figure 3.

Seasonal variation in the estimated proportions of the three HA classes in infected individuals as a function of time (in weeks) and across years (2002–2009). Continuous lines represent the estimated proportions of each class in infected individuals, the 95% CI are represented by the shaded areas. The H1 class is represented in red, the H3 class in black and the H11 class in green.