Early exposure to ultraviolet-B radiation decreases immune function later in life

Abstract

Amphibians have declined dramatically worldwide. Many of these declines are occurring in areas where no obvious anthropogenic stressors are present. It is proposed that in these areas, environmental factors such as elevated solar ultraviolet-B (UV-B) radiation could be responsible. Ultraviolet-B levels have increased in many parts of the world as a consequence of the anthropogenic destruction of the ozone layer. Amphibian tadpoles are particularly sensitive to the damaging effects of UV-B radiation, with exposure disrupting growth and fitness in many species. Given that UV-B can disrupt immune function in other animals, we tested the hypothesis that early UV-B exposure suppresses the immune responses of amphibian tadpoles and subsequent juvenile frogs. We exposed Limnodynastes peronii tadpoles to sublethal levels of UV-B radiation for 6 weeks after hatching, then examined indices of immune function in both the tadpoles and the subsequent metamorphs. There was no significant effect of UV-B on tadpole leucocyte counts or on their response to an acute antigen (phytohaemagglutinin) challenge. However, early UV-B exposure resulted in a significant reduction in both metamorph leucocyte abundance and their response to an acute phytohaemagglutinin challenge. These data demonstrate that early UV-B exposure can have carry-over effects on later life-history traits even if the applied stressor has no immediately discernible effect. These findings have important implications for our understanding of the effects of UV-B exposure on amphibian health and susceptibility to diseases such as chytridiomycosis.

Keywords: Amphibian declines; disease; immunocompetence; leucocyte; phytohaemagglutinin; ultraviolet radiation.

Figure 1:

The mean length (in millimetres) of Limnodynastes peronii tadpoles in the ultraviolet-B (UV-B) treatment (n = 48) or control treatment (n = 36) measured at three different time points during development. There was no significant effect of larval UV-B exposure on growth rates (F_1,19= 2.68, P = 0.12). Data are presented as mean values ± SEM.

Figure 2:

The standard metabolic rate (${\dot{V}}_{{\mathrm{O}}_2}$; in millilitres of O₂ per hour) of L. peronii tadpoles exposed to control and UV-B treatments measured during the initial stage of exposure (A; experienced from week 0 to 3 of the exposure period; absolute irradiance of UV-B during peak = 12.9 ± 3.18 µW cm⁻²; control, n = 28 and UV-B, n = 35) and during the final stage of exposure (B; experienced from week 3 to 6 of the exposure period; absolute irradiance of UV-B during peak = 18.41 ± 3.55 µW cm⁻²; control, n = 27 and UV-B, n = 25). There was no significant effect of larval UV-B exposure on standard metabolic rate rate at either the initial or the final stage of the exposure period. Data are presented as mean values + SEM.

Figure 3:

(A) The mean maximal tail swelling response (in millimetres) to phytohaemagglutinin administration in L. peronii tadpoles in the control treatment (n = 6) and UV-B treatment (n = 8). (B) The mean percentage of leucocytes per 200 blood cells in tadpoles exposed to the control treatment (n = 15) and UV-B treatment (n = 19). There was no significant effect of UV-B exposure on either parameter. Data are presented as mean values + SEM.

Figure 4:

(A) The mean maximal thigh swelling response (in millimetres) to phytohaemagglutinin injection of L. peronii metamorphs in the control treatment (n = 4) and UV-B treatment (n = 6) during development as tadpoles. (B) The mean percentage of leucocytes of L. peronii metamorphs in the UV-B treatment (n = 11) and control treatment (n = 8) during development as tadpoles. The maximal response to phytohaemagglutinin was greatest in the metamorphs from the control treatment group (F_1,8 = 0.93, P = 0.002). The proportion of leucocytes was also greatest in the control treatment group (F_1,17 = 5.6, P = 0.03). *Significant difference (P < 0.05) between the UV-B and control treatment groups.