Minor differences in body condition and immune status between avian influenza virus-infected and noninfected mallards: a sign of coevolution?

Wildlife pathogens can alter host fitness. Low pathogenic avian influenza virus (LPAIV) infection is thought to have negligible impacts on wild birds; however, effects of infection in free-living birds are largely unstudied. We investigated the extent to which LPAIV infection and shedding were associated with body condition and immune status in free-living mallards (Anas platyrhynchos), a partially migratory key LPAIV host species. We sampled mallards throughout the species' annual autumn LPAIV infection peak, and we classified individuals according to age, sex, and migratory strategy (based on stable hydrogen isotope analysis) when analyzing data on body mass and five indices of immune status. Body mass was similar for LPAIV-infected and noninfected birds. The degree of virus shedding from the cloaca and oropharynx was not associated with body mass. LPAIV infection and shedding were not associated with natural antibody (NAbs) and complement titers (first lines of defense against infections), concentrations of the acute phase protein haptoglobin (Hp), ratios of heterophils to lymphocytes (H:L ratio), and avian influenza virus (AIV)-specific antibody concentrations. NAbs titers were higher in LPAIV-infected males and local (i.e., short distance) migrants than in infected females and distant (i.e., long distance) migrants. Hp concentrations were higher in LPAIV-infected juveniles and females compared to infected adults and males. NAbs, complement, and Hp levels were lower in LPAIV-infected mallards in early autumn. Our study demonstrates weak associations between infection with and shedding of LPAIV and the body condition and immune status of free-living mallards. These results may support the role of mallards as asymptomatic carriers of LPAIV and raise questions about possible coevolution between virus and host

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

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

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

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

Mallards Feed Longer to Maintain Intake Rate under Competition on a Natural Food Distribution

Animals foraging in groups may benefit from a faster detection of food and predators, but competition by conspecifics may reduce intake rate. Competition may also alter the foraging behaviour of individuals, which can be influenced by dominance status and the way food is distributed over the environment. Many studies measuring the effects of competition and dominance status have been conducted on a uniform or highly clumped food distribution, while in reality prey distributions are often in-between these two extremes. The few studies that used a more natural food distribution only detected subtle effects of interference and dominance. We therefore conducted an experiment on a natural food distribution with focal mallards Anas platyrhynchos foraging alone and in a group of three, having a dominant, intermediate or subordinate dominance status. In this way, the foraging behaviour of the same individual in different treatments could be compared, and the effect of dominance was tested independently of individual identity. The experiment was balanced using a 4 x 4 Latin square design, with four focal and six non-focal birds. Individuals in a group achieved a similar intake rate (i.e. number of consumed seeds divided by trial length) as when foraging alone, because of an increase in the proportion of time feeding (albeit not significant for subordinate birds). Patch residence time and the number of different patches visited did not differ when birds were foraging alone or in a group. Besides some agonistic interactions, no differences in foraging behaviour between dominant, intermediate and subordinate birds were measured in group trials. Possibly group-foraging birds increased their feeding time because there was less need for vigilance or because they increased foraging intensity to compensate for competition. This study underlines that a higher competitor density does not necessarily lead to a lower intake rate, irrespective of dominance status

An additional field method to sex adult Barn Swallows during the non-breeding season in Zambia: white spot length in the outer tail feather

Adult Barn Swallows Hirundo rustica exhibit strong sexual size dimorphism in the length of the outermost tail feathers, which are longer in males compared with females. This trait is traditionally used to sex adult Barn Swallows in the field. However, due to the wear and breakage of the tips of the outer tail feather and tail moult during the non-breeding season, sexing becomes unreliable or even impossible. We therefore tested whether the length of the white spot on the outer tail feather is sexually dimorphic, and whether it can be used as an additional sexing method for adult Barn Swallows. The white spot length was sexually dimorphic, based on DNA analysis of 101 adult individuals caught at their roost during the non-breeding season in Zambia. Accuracy in sex determination of 95% could be obtained by classifying individuals with a white spot length <17.5 mm as females and those with a white spot length >29.5 mm as males. When applying the length of the white spot as an additional method to sex adult Barn Swallows on all birds caught in Zambia during the study period (N = 759), the percentage of birds that could successfully be sexed increased to more than 55%. Therefore we emphasise the importance of measuring the white spot length in addition to the tail fork depth and tail length to sex adult Barn Swallows in the non-breeding season.