Highly Pathogenic Avian Influenza Virus H5N1 Infection in a Long-Distance Migrant Shorebird under Migratory and Non-Migratory States

Corticosterone regulates physiological changes preparing wild birds for migration. It also modulates the immune system and may lead to increased susceptibility to infection, with implications for the spread of pathogens, including highly pathogenic avian influenza virus (HPAIV) H5N1. The red knot (Calidris canutus islandica) displays migratory changes in captivity and was used as a model to assess the effect of high plasma concentration of corticosterone on HPAIV H5N1 infection. We inoculated knots during pre-migration (N = 6), fueling (N = 5), migration (N = 9) and post-migration periods (N = 6). Knots from all groups shed similar viral titers for up to 5 days post-inoculation (dpi), peaking at 1 to 3 dpi. Lesions of acute encephalitis, associated with virus replication in neurons, were seen in 1 to 2 knots per group, leading to neurological disease and death at 5 to 11 dpi. Therefore, the risk of HPAIV H5N1 infection in wild birds and of potential transmission between wild birds and poultry may be similar at different times of the year, irrespective of wild birds' migratory status. However, in knots inoculated during the migration period, viral shedding levels positively correlated with pre-inoculation plasma concentration of corticosterone. Of these, knots that did not become productively infected had lower plasma concentration of corticosterone. Conversely, elevated plasma concentration of corticosterone did not result in an increased probability to develop clinical disease. These results suggest that birds with elevated plasma concentration of corticosterone at the time of migration (ready to migrate) may be more susceptible to acquisition of infection and shed higher viral titers—before the onset of clinical disease—than birds with low concentration of corticosterone (not ready for take-off). Yet, they may not be more prone to the development of clinical disease. Therefore, assuming no effect of sub-clinical infection on the likelihood of migratory take-off, this may favor the spread of HPAIV H5N1 by migratory birds over long distances

Biological Earth observation with animal sensors

Space-based tracking technology using low-cost miniature tags is now delivering data on fine-scale animal movement at near-global scale. Linked with remotely sensed environmental data, this offers a biological lens on habitat integrity and connectivity for conservation and human health; a global network of animal sentinels of environmen-tal change

Long flights do not influence immune responses of a long-distance migrant bird: a wind-tunnel experiment

Heavy physical work can result in physiological stress and suppressed immune function. Accordingly, long-distance migrant birds that fly for thousands of km within days can be expected to show immunosuppression, and hence be more vulnerable to infections en route. The red knot Calidris canutus Linnaeus is a long-distance migrant shorebird. We flew red knots the equivalent of 1500 km over 6 days in a wind tunnel. The humoral and cell-mediated immune responses of the flyers were compared to those of non-flying controls. Humoral immunity was measured as antibody production against injected diphtheria and tetanus antigens, and cell-mediated response as phytohemagglutinin-induced wing-web swelling. Blood corticosterone levels, which may modulate immune function, were measured in parallel. The long flights had no detectable effects on humoral or cell-mediated immune responses, or on corticosterone levels. Thus, flight performance per se may not be particularly stressful or immunosuppressive in red knots. Some birds assigned as flyers refused to fly for extended periods. Before flights started, these non-flyers had significantly lower antibody responses against tetanus than the birds that carried out the full flight program. This suggests that only birds in good physical condition may be willing to take on heavy exercise. We conclude that these long-distance migrants appear well adapted to the work load induced by long flights, enabling them to cope with long flight distances without increased stress levels and suppression of immunity. Whether this also applies in the wild, where the migrating birds may face adverse weather and food conditions, remains to be investigated.

Wintering ground data from migratory willow warblers

This file contains data collected from migratory willow warblers (Phylloscopus trochilus) on their wintering grounds in Zambia. Data includes malaria prevalence and intensity, feather quality variables, corticosterone, stable hydrogen isotope analysis of feathers (H), and body size measurements

Data from: Migration distance does not predict blood parasitism in a migratory songbird

Migration can influence host-parasite dynamics in animals by increasing exposure to parasites, by reducing the energy available for immune defence, or by culling of infected individuals. These mechanisms have been demonstrated in several comparative analyses; however, few studies have investigated whether conspecific variation in migration distance may also be related to disease susceptibility. Here, we ask whether autumn migration distance, inferred from stable hydrogen isotope analysis of summer-grown feathers (δ2Hf) in Europe, correlates with blood parasite prevalence and intensity of infection for willow warblers (Phylloscopus trochilus) wintering in Zambia. We also investigated whether infection was correlated with individual condition (assessed via corticosterone, scaled mass index, and feather quality). We found that 43% of birds were infected with Haemoproteus palloris (lineage WW1). Using generalized linear models, we found no relationship between migration distance and either Haemoproteus infection prevalence or intensity. There was spatial variation in breeding ground origins of infected vs. non-infected birds, with infected birds originating from more northern sites than non-infected birds, but this difference translated into only slightly longer estimated migration distances (~214 km) for infected birds. We found no relationship between body condition indices and Haemoproteus infection prevalence or intensity. Our results do not support any of the proposed mechanisms for migration effects on host-parasite dynamics, and cautiously suggest that other factors may be more important for determining individual susceptibility to disease in migratory bird species

Data from: Migration distance does not predict blood parasitism in a migratory songbird

Migration can influence host-parasite dynamics in animals by increasing exposure to parasites, by reducing the energy available for immune defence, or by culling of infected individuals. These mechanisms have been demonstrated in several comparative analyses; however, few studies have investigated whether conspecific variation in migration distance may also be related to disease susceptibility. Here, we ask whether autumn migration distance, inferred from stable hydrogen isotope analysis of summer-grown feathers (δ2Hf) in Europe, correlates with blood parasite prevalence and intensity of infection for willow warblers (Phylloscopus trochilus) wintering in Zambia. We also investigated whether infection was correlated with individual condition (assessed via corticosterone, scaled mass index, and feather quality). We found that 43% of birds were infected with Haemoproteus palloris (lineage WW1). Using generalized linear models, we found no relationship between migration distance and either Haemoproteus infection prevalence or intensity. There was spatial variation in breeding ground origins of infected vs. non-infected birds, with infected birds originating from more northern sites than non-infected birds, but this difference translated into only slightly longer estimated migration distances (~214 km) for infected birds. We found no relationship between body condition indices and Haemoproteus infection prevalence or intensity. Our results do not support any of the proposed mechanisms for migration effects on host-parasite dynamics, and cautiously suggest that other factors may be more important for determining individual susceptibility to disease in migratory bird species

Guillemot measurements

Biometry, phenology and CORT measurements of adult and juvenile common guillemots on Hornøy

Cod larvae abundances

Abundances and weights of cod larvae from different spawning grounds around the guillemot colony at Hornøya, by date and yea

Significant differences in migratory state and constitutive immunity in red knots inoculated with highly pathogenic avian influenza virus (HPAIV) H5N1.

<p>I: knots inoculated during the pre-migration period (N = 6); II: knots inoculated during the fueling period (N = 5); III: knots inoculated during the migration period (N≤12); IV: knots inoculated during the post-migration period (N = 6). The three negative control knots are included in the migration period group (III) for the analyses of pre-inoculation measures of body mass, constitutive immunity and plasma concentration of corticosterone, and of the measures of activity levels (N = 12); the necropsied negative control knot is included in the migration group (III) for the analyses of the measures of length and mass of organs (N = 10).</p

Pathology of highly pathogenic avian influenza virus H5N1 infection in red knots.

<p>Lesions of acute pancreatitis, showing a discrete focus of pancreatic exocrine cell necrosis (A); lesions of acute encephalitis, showing perivascular accumulation of lymphocytes (B); and presence of influenza virus antigen in nuclei of neurons (large cells) and glial cells (small cells; C). Slides were stained with hematoxylin and eosin (A and B), or by immunohistochemistry using a monoclonal antibody against the nucleoprotein of influenza A virus as the primary antibody (C).</p