Bird population declines due to radiation exposure at Chernobyl are stronger in species with pheomelanin-based coloration

Eumelanin and pheomelanin are the most common pigments providing color to the integument of vertebrates. While pheomelanogenesis requires high levels of a key intracellular antioxidant (glutathione, GSH), eumelanogenesis is inhibited by GSH. This implies that species that possess the molecular basis to produce large amounts of pheomelanin might be more limited in coping with environmental conditions that generate oxidative stress than species that produce eumelanin. Exposure to ionizing radiation produces free radicals and depletes antioxidant resources. GSH is particularly susceptible to radiation, so that species with large proportions of pheomelanic integument may be limited by the availability of GSH to combat oxidative stress and may thus suffer more from radiation effects. We tested this hypothesis in 97 species of birds censused in areas with varying levels of radioactive contamination around Chernobyl. After controlling for the effects of carotenoid-based color, body mass and similarity among taxa due to common phylogenetic descent, the proportion of pheomelanic plumage was strongly negatively related to the slope estimates of the relationship between abundance and radiation levels, while no effect of eumelanic color proportion was found. This represents the first report of an effect of the expression of melanin-based coloration on the capacity to resist the effects of ionizing radiation. Population declines were also stronger in species that exhibit carotenoid-based coloration and have large body mass. The magnitude of population declines had a relatively high phylogenetic signal, indicating that certain groups of birds, especially non-corvid passeriforms, are particularly susceptible to suffer from the effects of radioactive contamination due to phylogenetic inertia.