Increased tolerance to ultraviolet radiation (UVR) and cotolerance to cadmium in UVR-acclimatized freshwater periphyton

We studied the long-term acclimatization of freshwater periphyton communities exposed to low and high ultraviolet radiation (UVR) intensities that simulate UVR doses received by lowland and high-mountain streams of central Europe. To assess changes induced by UVR, we compared the community structure (species and biomass), function (photosynthetic yield), and tolerance to UVR and cadmium of periphyton growing in microcosms (artificial channels). On the basis of the rationale behind the pollution-induced community tolerance concept, we expected that an increase in UVR tolerance would be through the replacement of more sensitive taxa by more tolerant taxa. After 38 d of exposure, periphyton in the high-UVR treatment was dominated by Cyanobacteria, whereas diatoms dominated periphyton in the low-UVR treatment. Concomitantly, the highUVR community increased its tolerance to UVR and showed cotolerance to cadmium (Cd). Structural changes contributing to this increased tolerance included an increase in UVR-absorbing compounds, and the formation of cell aggregates that increased self shading. Induction of antioxidant enzymes after UVR and Cd exposure might be involved as defense mechanisms against oxidative stress. These changes reduced the exposure and effects of UVR, resulting in the protection of photosynthesis (high-UVR photosynthetic yield was unaffected). A fivefold reduction in chlorophyll a in the high-UVR treatment suggested that acclimatization had high metabolic costs. Additional experiments showed that even though biomass accrual offered some protection against UVR and Cd, the community changes experienced by the high-UVR community contributed the most to UVR tolerance. Periphyton exposed to high UVR may experience simultaneous positive (tolerance to UVR and cotolerance to Cd) and negative effects (biomass reduction can increase accessibility by toxicants). Among risks posed by global change, the interaction between ozone depletion and climate change may enhance the exposure of aquatic communities to ultraviolet radiation (UVR, 280–400 nm) (Villafane et al. 2007). In aquatic photosynthetic organisms, enhanced UVR can induce a broad range of cellular effects, depending on light quality, intensity, and exposure (Häder et al. 2003). Besides direct biological effects (Helbling et al. 2001), UVR can cause cellular damage indirectly, through increased production of reactive oxygen, which may result in increasing oxidative stress (Helbling et al. 2001; Hernando et al. 2005). Ensuing physiological consequences on photosynthesis and growth (Holzinger and Lutz 2006) suggest that a continued increase in solar UVR can, in the long term, result in reduced primary production and a change in phytoplankton and periphyton composition (Häder et al. 1998). Algae have evolved a variety of protective strategies to attenuate cellular UV absorption (Häder et al. 1998; Navarro et al. 2007), neutralize oxygen radicals (Ledford and Niyogi 2005), and repair damaged molecules (Jansen et al. 1999). Preventive defense mechanisms of algae include the production of UV-absorbing compounds (Sommaruga and Garcia-Pichel 1999; Tank et al. 2003; Navarro et al. 2007), and reactive oxygen scavengers as well as enzymes that participate in cellular antioxidant-scavenging cycles (Aguilera et al. 2002). Other mechanisms operate to repair damages to DNA or the photosynthetic apparatus (Bouchard et al. 2006; Häder and Sinha 2005) once damages have occurred. However, specific algae differ in their sensitivity to UVR (Donahue et al. 2003; Xue et al. 2005); thus the degree of response by periphyton to enhanced UVR will depend on community composition (Weidman et al. 2005) as well as UVR exposure history. For instance, studies of UVR effects on periphyton document large differences in response by communities from different environments (Kelly et al. 2003; Tank and Schindler 2004). The pollution-induced community tolerance (PICT) concept predicts a community that has been restructured upon chronic chemical stress to become more tolerant to that chemical (Blanck et al. 1988). Elimination of sensitive species, replacement by more tolerant ones, and individual biochemical acclimatization can all contribute to increase tolerance to a chemical stress (Blanck 2002; Schmitt et al. 2006). On the basis of the rationale of PICT, UVR-induced structural changes are anticipated to increase the tolerance of the periphyton community to enhanced UVR. In their 1 Corresponding author ([email protected]).