Contrasting Responses of Marine and Freshwater Photosynthetic Organisms to UVB Radiation: A Meta-Analysis

Abstract

Ultraviolet-B (UVB) radiation is a global stressor that has profound impacts on freshwater and marine ecosystems. However, an analysis of the patterns of sensitivity to UVB radiation across aquatic photosynthetic organisms has not yet been published. Here, we performed a meta-analysis on results reported in 214 studies compiled from the published literature to quantify and compare the magnitude of responses of aquatic photosynthetic organisms to changes in UVB radiation. The meta-analysis was conducted on observations of marine (n = 893) and freshwater macroalgae (n = 126) and of marine (n = 1,087) and freshwater (n = 2,889) microalgae (total n = 4,995). Most of these studies (85%) analyzed the performance of organisms exposed to natural solar radiation when UVB was partially or totally reduced compared with the organismal performance under the full solar radiation spectrum, whereas the remaining 15% of the studies examined the responses of organisms to elevated UVB radiation mostly using artificial lamps. We found that marine photosynthetic organisms tend to be more sensitive than freshwater photosynthetic organisms to UVB radiation; responses to either decreased or increased UVB radiation vary among taxa; the mortality rate is the most sensitive of the trait responses to elevated UVB radiation, followed by changes in cellular and molecular traits; the sensitivity of microalgae to UVB radiation is dependent on size, with small-celled microalgae more sensitive than large-celled microalgae to UVB radiation. Thick macroalgae morphotypes were the less sensitive to UVB, but this effect could not be separated from phylogenetic differences. The high sensitivity of marine species, particularly the smallest photosynthetic organisms, to increased UVB radiation suggests that the oligotrophic ocean, a habitat comprising 70% of the world's oceans with high UVB penetration and dominated by picoautotrophs, is extremely vulnerable to changes in UVB radiation.

Increasing temperature within thermal limits compensates negative ultraviolet‐B radiation effects in terrestrial and aquatic organisms

“…Our study indicated that terrestrial organisms are the most resilient to increased UV‐B radiation, followed by freshwater and marine organisms, which is in agreement with a previous meta‐analysis that investigated UV‐B effects on photoautotrophs (Jin et al, ). Early‐life stages such as embryos and larvae are often translucent, and although many harbour photoprotective compounds, they remain particularly vulnerable to UV radiation (Aranda et al, ; Llabres et al, ; Overmans et al, ), consistent with our findings.…”

“…Although previous meta‐analyses demonstrated that the magnitude of drivers or stressors (e.g., pH change, Kroeker et al, ) or the duration of experiments (e.g., from hours to ~ 400 days, Kroeker et al, ) did not consistently explain a significant amount of variability, the magnitude of UV‐B radiation change does influence responses of marine (Llabres et al, ) and aquatic photosynthetic organisms (Jin et al, ). Our study demonstrates that the relationship between biological responses and the magnitude of temperature/UV‐B change is weak based on the whole dataset, and these overall effects vary greatly between response levels (Supporting Information Figure S2).…”

“…Hence, a number of experiments have been conducted to understand the response of terrestrial, freshwater and marine organisms to the combined effects of warming and elevated UV‐B radiation. Their vulnerability to rising temperature and UV‐B radiation as isolated stressors has been analysed in several reports and reviews (Bais et al, ; Caldwell et al, ; Hader et al, ; Hoegh‐Guldberg & Bruno, ; Wernberg et al, ) and meta‐analyses (Bancroft, Baker, & Blaustein, ; Jin, Duarte, & Agusti, ; Llabres et al, ; Peng, Liao, Zhou, & Peng, ).…”

“…UV‐B radiation is mutagenic and harmful for organisms and is considered an evolutionary and selective force (Rothschild, ; Rozema et al, ), and thus geographical and habitat asymmetries in UV‐B exposure influence patterns of organism sensitivity, as described in different studies (Agusti, Llabres, Carreja, Fernandez, & Duarte, ; Llabres et al, ; Paul & Gwynn‐Jones, ). In addition, previous meta‐analyses showed that (a) marine photosynthetic organisms tend to be more sensitive to UV‐B radiation than their freshwater counterparts (Jin et al, ), (b) marine organisms from the Southern Hemisphere are more resistant to UV‐B radiation than those from the Northern Hemisphere, which is forced by stratospheric ozone asymmetries between hemispheres (Agusti et al, ), and (c) marine photosynthetic organisms are less sensitive to UV‐B than marine animals (Agusti et al, ). In addition, the responses to UV‐B radiation largely depend on the magnitude of UV‐B level, such that the impacts of UV‐B increase with dose (Llabres et al, ; Peng et al, ).…”

The antagonistic effect of UV radiation on warming or nitrate enrichment depends on ecotypes of freshwater macroalgae (Charophytes)

“…Therefore, to develop an experiment on interactive effects, we should consider not only the different responses of species (e.g., Roleda ) but also the origin of populations as confirmed by the meta‐analysis by Jin et al. () on the photosynthetic organism's response to UVR. Related to this, studies were carried out on the intraspecific differences in phenotypic plasticity of the macrophyte Ceratophyllum demersum (Hyldgaard and Brix ), or how the concomitant positive effect of an increase in T and N can occur depending on the charophyte population origin (Puche et al.…”