Pathogen dynamics in a partial migrant: Interactions between mallards (Anas platyrhynchos) and avian influenza viruses

Abstract

Zoonotic pathogens may pose a serious threat for humans, requiring a better understanding of the ecology and transmission of these pathogens in their natural (wildlife) hosts. The zoonotic pathogen studied in this thesis is low pathogenic avian influenza virus (LPAIV). This pathogen circulates naturally in wild birds, causing no or limited signs of disease. Birds of wetlands and aquatic environments (orders Anseriformes and Charadriiformes) are considered the main LPAIV reservoir. The aim of this study was to advance our knowledge of the ecological processes underlying the epidemiology of LPAIVs in wild birds, by investigating the host-pathogen interaction between a free-living key LPAIV host species, the mallard (Anas platyrhynchos), and LPAIV at a local scale (i.e. duck decoy: swim-in traps connected to a large pond) in the Netherlands. Throughout a complete annual cycle, we comprehensively sampled mallards measuring both current and past infection (i.e. LPAIV prevalence and AIV antibody prevalence, respectively). We demonstrated a minor LPAIV infection peak in summer and a dominant peak in autumn, whereas prevalence of antibodies against AIV peaked in winter and spring. The summer LPAIV infection peak was likely driven by the entrance of unfledged naïve juveniles into the resident population, as they were more likely to be infected, shed higher quantities of virus and were less likely to have AIV antibodies than adults. Still, we discovered that in this period nearly half of the mallard eggs received maternal AIV antibodies, which may grant neonates protection against LPAIV infection early in life. The large autumn LPAIV infection peak was likely driven by the arrival of susceptible migratory mallards on the wintering grounds, since they were more likely to be infected than residents and showed low AIV antibody prevalence. Throughout Europe mallards are partially migratory, meaning that the population consist of both migratory and resident birds, which mix at the wintering grounds, like the Netherlands, in autumn and winter. We distinguished between migratory and resident mallards, using hydrogen stable isotopes (δ2H) in their feathers. The LPAIV infection peak in autumn was likely initiated by a single introduction of an LPAIV subtype H3 in susceptible residents, after which migrants likely acted as local amplifiers to maintain this epizootic. But whether migratory birds also acted as a vector, importing novel LPAIV strains from afar, is less clear. Additionally, we investigated potential effects of LPAIV infection on body mass, immune status and movement behaviour of free-living mallards. Body mass and five immunological indices differed only marginally between LPAIV infected and non-infected individuals. This raises the intriguing notion that this may be a consequence of host-pathogen co-evolution, explaining the alleged role of mallards as a key reservoir of LPAIV. Daily regional movements of LPAIV infected mallards were lower than those of non-infected individuals, which became increasingly lower when weather conditions worsened. LPAIV infected mallards are probably still capable of transporting viral particles to other areas, although the distance of spread might be lower than one might expect from the behaviour of non-infected individuals.