Ecologic Immunology of Avian Influenza (H5N1) in Migratory Birds

European Commission's Joint Research Centre, Ispra, Italy.
Emerging infectious diseases (Impact Factor: 6.75). 09/2007; 13(8):1139-43. DOI: 10.3201/eid1308.070319
Source: PubMed


The claim that migratory birds are responsible for the long-distance spread of highly pathogenic avian influenza viruses of subtype H5N1 rests on the assumption that infected wild birds can remain asymptomatic and migrate long distances unhampered. We critically assess this claim from the perspective of ecologic immunology, a research field that analyzes immune function in an ecologic, physiologic, and evolutionary context. Long-distance migration is one of the most demanding activities in the animal world. We show that several studies demonstrate that such prolonged, intense exercise leads to immunosuppression and that migratory performance is negatively affected by infections. These findings make it unlikely that wild birds can spread the virus along established long-distance migration pathways. However, infected, symptomatic wild birds may act as vectors over shorter distances, as appears to have occurred in Europe in early 2006.

Download full-text


Available from: Nikolaos I Stilianakis, Oct 01, 2015
21 Reads
  • Source
    • "Novel areas might also contain pathogens with altered virulence (relative to the range core), as an adaptation to altered host density, or from spatial sorting on the pathogens themselves (Phillips & Puschendorf 2013). Fourth, the physical exertion of sustained, rapid movement through unfamiliar habitat is likely to produce tissue damage and elevated stress levels (Segerstrom 2007; Weber & Stilianakis 2007; Buehler et al. 2010). Under these conditions, immune responses may be modified to prevent autoimmune damage (Pedersen & Hoffman-Goetz 2000; Raberg et al. 2002; Brown & Shine 2014). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Because an individual's investment into the immune system may modify its dispersal rate, immune function may evolve rapidly in an invader. We collected cane toads (Rhinella marina) from sites spanning their 75-year invasion history in Australia, bred them, and raised their progeny in standard conditions. Evolved shifts in immune function should manifest as differences in immune responses among the progeny of parents collected in different locations. Parental location did not affect the offspring's cell-mediated immune response or stress response, but blood from the offspring of invasion-front toads had more neutrophils, and was more effective at phagocytosis and killing bacteria. These latter measures of immune function are negatively correlated with rate of dispersal in free-ranging toads. Our results suggest that the invasion of tropical Australia by cane toads has resulted in rapid genetically based compensatory shifts in the aspects of immune responses that are most compromised by the rigours of long-distance dispersal.
    Ecology Letters 11/2014; 18(1):n/a-n/a. DOI:10.1111/ele.12390 · 10.69 Impact Factor
  • Source
    • "In areas commonly affected by HPAI, poultry trade is regarded as the primary cause for the persistence and spread of HPAI (Gauthier-Clerc et al., 2007), and long-distance transportation of poultry products along with unregulated practices at poultry markets have been linked to outbreaks in many parts of Asia (Amonsin et al., 2008; Liu et al., 2003; Shortridge et al., 1998; Wang et al., 2006; Yu et al., 2007). Waterbirds (i.e., Anatidae and Charadriidae) have been identified as primary reservoirs for low pathogenic influenza viruses (Stallknecht and Shane, 1988), but with our limited knowledge about the distances infected birds migrate and connectivity among populations, the importance of HPAI transmission by wild birds remains an open question (Gaidet et al., 2010; Takekawa et al., 2010b; van Gils et al., 2007; Weber and Stilianakis, 2007). The potential of wild birds to spread HPAI is evident in the 2005 outbreak at Qinghai Lake in China that killed more than 6000 wild waterfowl. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Satellite-based tracking of migratory waterfowl is an important tool for understanding the potential role of wild birds in the long-distance transmission of highly pathogenic avian influenza. However, employing this technique on a continental scale is prohibitively expensive. This study explores the utility of stable isotope ratios in feathers in examining both the distances traveled by migratory birds and variation in migration behavior. We compared the satellite-derived movement data of 22 ducks from 8 species captured at wintering areas in Bangladesh, Turkey, and Hong Kong with deuterium ratios (δD) in the feathers of these and other individuals captured at the same locations. We derived likely molting locations from the satellite tracking data and generated expected isotope ratios based on an interpolated map of δD in rainwater. Although δD was correlated with the distance between wintering and molting locations, surprisingly, measured δD values were not correlated with either expected values or latitudes of molting sites. However, population-level parameters derived from the satellite-tracking data, such as mean distance between wintering and molting locations and variation in migration distance, were reflected by means and variation of the stable isotope values. Our findings call into question the relevance of the rainfall isotope map for Asia for linking feather isotopes to molting locations, and underscore the need for extensive ground truthing in the form of feather-based isoscapes. Nevertheless, stable isotopes from feathers could inform disease models by characterizing the degree to which regional breeding populations interact at common wintering locations. Feather isotopes also could aid in surveying wintering locations to determine where high-resolution tracking techniques (e.g. satellite tracking) could most effectively be employed. Moreover, intrinsic markers such as stable isotopes offer the only means of inferring movement information from birds that have died as a result of infection. In the absence of feather based-isoscapes, we recommend a combination of isotope analysis and satellite-tracking as the best means of generating aggregate movement data for informing disease models.
    Ecological Indicators 10/2014; 45:266–273. DOI:10.1016/j.ecolind.2014.04.027 · 3.44 Impact Factor
  • Source
    • "Knowledge of nutritional effects on immune defence is particularly lacking in field populations (Boggs, 2009), and even more so in migrating animals such as locusts (Weber and Stilianakis, 2007). In a closely related species, field populations of the Mormon cricket (Anabrus simplex) were found to be generally protein-deficient , and it is this deficiency that induced the marching behaviour in these species (Simpson et al., 2006). "
    [Show abstract] [Hide abstract]
    ABSTRACT: There is growing evidence to suggest that hosts can alter their dietary intake to recoup the specific resources involved in mounting effective resistance against parasites and pathogens. We examined macronutrient ingestion and disease-resistance in the Australian plague locust (Chortoicetes terminifera), challenged with a fungal pathogen (Metarhizium acridum) under dietary regimes varying in their relative amounts of protein and digestible carbohydrate. Dietary protein influenced constitutive immune function to a greater extent than did carbohydrate, indicating higher protein costs of mounting an immune defence than carbohydrate or overall energy costs. However, it appears that increased immune function, as a result of greater protein ingestion, was not sufficient to protect locusts from fungal disease. We found that locusts restricted to diets high in protein (P) and low in carbohydrate (C) were more likely to die of a fungal infection than those restricted to diets with a low P:C ratio. We hypothesise that the fungus is more efficient at exploiting protein in the insect's haemolymph than the host is at producing immune effectors, tipping the balance in favour of the pathogen on high-protein diets. When allowed free-choice, survivors of a fungus-challenge chose a less-protein-rich diet than those succumbing to infection and those not challenged with fungus locusts. These results are contrary to previous studies on caterpillars in the genus Spodoptera challenged with bacterial and baculoviral pathogens, indicating that nutrient ingestion and pathogen resistance may be a complex interaction specific to different host species and disease agents.
    Journal of Insect Physiology 05/2014; 69. DOI:10.1016/j.jinsphys.2014.05.015 · 2.47 Impact Factor
Show more