Antioxidants, radiation and mutation as revealed by sperm abnormality in barn swallows from Chernobyl

Abstract

Reduced levels of antioxidants such as carotenoids and vitamins A and E can increase DNA damage caused by free radicals. Exposure to radiation has been proposed to reduce levels of antioxidants that are used for DNA repair and this reduction may be responsible for increased levels of mutation in radioactively contaminated areas. We test this hypothesis using field measures of antioxidants in blood, liver and eggs of the barn swallow Hirundo rustica while relating these to levels of mutation as reflected by the frequency of abnormal sperm. Antioxidant levels in blood, liver and eggs were reduced in Chernobyl, Ukraine, compared with an uncontaminated control area, and levels of antioxidants correlated negatively with levels of background radiation. The frequency of abnormal sperm was almost an order of magnitude higher in Chernobyl than in the control area and was negatively related to antioxidant levels in blood and liver. This is consistent with the hypothesis of a direct link between radiation and individual levels of antioxidants, suggesting that levels of mutation differ among individuals owing to individual differences in the abundance of antioxidants.

Figure 1

Concentration of antioxidants (μgg⁻¹) in (a) blood and (b) liver of adult barn swallows and in (c) eggs of barn swallows from Chernobyl (grey bars) and Kanev (open bars; uncontaminated control area). Values are means (+1s.e.). One-way ANOVAs revealed significant differences for blood ((a) F=18.58, d.f.=1,39, p < 0.001; F=16.64, d.f.=1,39, p=0.0002; F=16.64, d.f.=1,39, p < 0.001, respectively); for liver retinol, α-tocopherol and carotenoids ((b) F=90.70, d.f.=1,56, p=0.001; F=22.33, d.f.=1,56, p < 0001; F=30.29, d.f.=1,56, p < 0.001, respectively); and for egg α-tocopherol and carotenoids ((c) F=9.23, d.f.=1,43, p=0.004; F=5.31, d.f.=1,43, p=0.03, respectively), while the difference for egg retinol was not significant (F=1.29, d.f.=1,43, p=0.26).

Figure 2

Antioxidants in liver of adult barn swallows from Ukraine in relation to levels of radiation (mRh⁻¹). The regressions were significant when radiation level was log-transformed ((a) retinol (μgg⁻¹): F=22.01, d.f.=1,56, r²=0.28, p < 0.0001, slope (s.e.)=−21.47 (4.58); (b) α-tocopherol (μgg⁻¹): F=11.84, d.f.=1,56, r²=0.17, p=0.001, slope (s.e.)=−7.00 (2.04); (c) carotenoids (μgg⁻¹): F=9.51, d.f.=1,56, r²=0.15, p=0.003, slope (s.e.)=−2.46 (0.80), respectively).

Figure 3

Frequency of abnormal sperm (%) in barn swallows from Ukraine in relation to radiation and liver antioxidants in adult males. The regressions were significant when radiation level was log-transformed ((a) radiation (mRh⁻¹); F=34.07, d.f.=1,34, r²=0.50, p < 0.0001, slope (s.e.)=0.21 (0.04); (b) retinol (μgg⁻¹): F=35.98, d.f.=1,34, r²=0.51, p < 0.0001, slope (s.e.)=−0.005 (0.001); (c) α-tocopherol (μgg⁻¹): F=71.86, d.f.=1,34, r²=0.68, p < 0.0001, slope (s.e.)=−0.014 (0.002); (d) carotenoids (μgg⁻¹): F=29.43, d.f.=1,34, r²=0.46, p < 0.0001, slope (s.e.)=−0.03 (0.01), respectively). Similar results were found for antioxidants in blood (linear regressions with radiation level log-transformed: retinol (μgg⁻¹): F=12.48, d.f.=1,26, r²=0.32, p=0.002, slope (s.e.)=−0.74 (0.21); (c) α-tocopherol (μgg⁻¹): F=11.33, d.f.=1,26, r²=0.25, p=0.006, slope (s.e.)=−0.07 (0.02); (d) carotenoids (μgg⁻¹): F=8.78, d.f.=1,26, r²=0.30, p=0.002, slope (s.e.)=−1.55 (0.46), respectively).