Defenses against keratinolytic bacteria in birds living in radioactively contaminated areas

Abstract

Microorganisms have shaped the evolution of a variety of defense mechanisms against pathogenic infections. Radioactivity modifies bacterial communities and, therefore, bird hosts breeding in contaminated areas are expected to adapt to the new bacterial environment. We tested this hypothesis in populations of barn swallows (Hirundo rustica) from a gradient of background radiation levels at Chernobyl and uncontaminated controls from Denmark. Investment in defenses against keratinolytic bacteria was measured from feather structure (i.e., susceptibility to degradation) and uropygial secretions. We studied degradability of tail feathers from areas varying in contamination in laboratory experiments using incubation of feathers with a feather-degrading bacterium, Bacillus licheniformis, followed by measurement of the amount of keratin digested. The size of uropygial glands and secretion amounts were quantified, followed by antimicrobial tests against B. licheniformis and quantification of wear of feathers. Feathers of males, but not of females, from highly contaminated areas degraded at a lower rate than those from medium and low contamination areas. However, feathers of both sexes from the Danish populations showed little evidence of degradation. Individual barn swallows from the more contaminated areas of Ukraine produced the largest uropygial secretions with higher antimicrobial activity, although wear of feathers did not differ among males from different populations. In Denmark, swallows produced smaller quantities of uropygial secretion with lower antimicrobial activity, which was similar to swallow populations from uncontaminated areas in Ukraine. Therefore, barn swallows breeding in contaminated areas invested more in all defenses against keratinolytic bacteria than in uncontaminated areas of Ukraine and Denmark, although they had similar levels of feather wear. Strong natural selection exerted by radioactivity may have selected for individuals with higher defense capacity against bacterial infections during the 30 years since the Chernobyl disaster.

Capacity of blood plasma is higher in birds breeding in radioactively contaminated areas

“…We have previously demonstrated that birds from heavily radioactively contaminated areas were those more resistant to feather degradation by keratinolytic bacteria [28]. Microbial communities in Chernobyl are altered and the phenotypic condition of hosts has deteriorated as a consequence of the nuclear accident (see Introduction).…”

“…Although individuals of the two sexes collaborate in nest building, females spend more time inside the nests (laying eggs and incubating them) than males [26]. In feathers, bacterial communities differ among the sexes [11], and also in some defences against keratinolytic degradation [28]. In addition, the investment in reproduction may be lower in contaminated than in clean areas, since barn swallows experience reduced reproductive success in Chernobyl [26].…”

“…megaterium . It is possible that for inhibiting feather-degrading microorganisms, other mechanisms such as uropygial secretions or physical resistance to degradation may be more developed [28]. Interestingly, both negative relationships between radiation and inhibition capacity were against L .…”

“…Alternatively, selective pressures exerted by evolving, more complex communities of microorganisms, together with high mortality rates in barn swallow hosts in Chernobyl [26], may have accelerated the process of adaptation in these bird populations. To date, there are very few examples of animals adapting to ionizing radiation in Chernobyl [27] but among these a higher level of resistance of feathers to degradation by keratinolytic bacteria was found in barn swallows living in more contaminated areas around Chernobyl [28]. In light of this prior finding, we predict that barn swallows in Chernobyl will be more resistant to bacterial infections than control populations given more than 30 years of selection following the accident.…”

Interspecific variation in deterioration and degradability of avian feathers: the evolutionary role of microorganisms

“…Moreover, since these environmental factors likely vary among species (see above), natural selection could have favoured the evolution of characteristics that counteract or reduce feather degradation by keratinolytic bacteria in environments that are distinctive of each species (Burtt , Burtt et al , Javůrková et al ). If this was the case, we should find interspecific variation in traits functioning in preventing feathers’ wear (Burtt ) such as feather susceptibility to degradation by keratinolytic bacteria (hereafter, feather degradability) (Ruiz‐De‐Castañeda et al , , Ruiz‐Rodríguez et al ).…”