Environmental effects of stratospheric ozone depletion, UV radiation and interactions with climate change: UNEP Environmental Effects Assessment Panel, update 2019.

This assessment, by the United Nations Environment Programme (UNEP) Environmental Effects Assessment Panel (EEAP), one of three Panels informing the Parties to the Montreal Protocol, provides an update, since our previous extensive assessment (Photochem. Photobiol. Sci., 2019, 18, 595-828), of recent findings of current and projected interactive environmental effects of ultraviolet (UV) radiation, stratospheric ozone, and climate change. These effects include those on human health, air quality, terrestrial and aquatic ecosystems, biogeochemical cycles, and materials used in construction and other services. The present update evaluates further evidence of the consequences of human activity on climate change that are altering the exposure of organisms and ecosystems to UV radiation. This in turn reveals the interactive effects of many climate change factors with UV radiation that have implications for the atmosphere, feedbacks, contaminant fate and transport, organismal responses, and many outdoor materials including plastics, wood, and fabrics. The universal ratification of the Montreal Protocol, signed by 197 countries, has led to the regulation and phase-out of chemicals that deplete the stratospheric ozone layer. Although this treaty has had unprecedented success in protecting the ozone layer, and hence all life on Earth from damaging UV radiation, it is also making a substantial contribution to reducing climate warming because many of the chemicals under this treaty are greenhouse gases.

Environmental effects of ozone depletion, UV radiation and interactions with climate change: UNEP Environmental Effects Assessment Panel, update 2017.

The Environmental Effects Assessment Panel (EEAP) is one of three Panels of experts that inform the Parties to the Montreal Protocol. The EEAP focuses on the effects of UV radiation on human health, terrestrial and aquatic ecosystems, air quality, and materials, as well as on the interactive effects of UV radiation and global climate change. When considering the effects of climate change, it has become clear that processes resulting in changes in stratospheric ozone are more complex than previously held. Because of the Montreal Protocol, there are now indications of the beginnings of a recovery of stratospheric ozone, although the time required to reach levels like those before the 1960s is still uncertain, particularly as the effects of stratospheric ozone on climate change and vice versa, are not yet fully understood. Some regions will likely receive enhanced levels of UV radiation, while other areas will likely experience a reduction in UV radiation as ozone- and climate-driven changes affect the amounts of UV radiation reaching the Earth's surface. Like the other Panels, the EEAP produces detailed Quadrennial Reports every four years; the most recent was published as a series of seven papers in 2015 (Photochem. Photobiol. Sci., 2015, 14, 1-184). In the years in between, the EEAP produces less detailed and shorter Update Reports of recent and relevant scientific findings. The most recent of these was for 2016 (Photochem. Photobiol. Sci., 2017, 16, 107-145). The present 2017 Update Report assesses some of the highlights and new insights about the interactive nature of the direct and indirect effects of UV radiation, atmospheric processes, and climate change. A full 2018 Quadrennial Assessment, will be made available in 2018/2019.

Solar ultraviolet radiation and ozone depletion-driven climate change: effects on terrestrial ecosystems.

In this assessment we summarise advances in our knowledge of how UV-B radiation (280-315 nm), together with other climate change factors, influence terrestrial organisms and ecosystems. We identify key uncertainties and knowledge gaps that limit our ability to fully evaluate the interactive effects of ozone depletion and climate change on these systems. We also evaluate the biological consequences of the way in which stratospheric ozone depletion has contributed to climate change in the Southern Hemisphere. Since the last assessment, several new findings or insights have emerged or been strengthened. These include: (1) the increasing recognition that UV-B radiation has specific regulatory roles in plant growth and development that in turn can have beneficial consequences for plant productivity via effects on plant hardiness, enhanced plant resistance to herbivores and pathogens, and improved quality of agricultural products with subsequent implications for food security; (2) UV-B radiation together with UV-A (315-400 nm) and visible (400-700 nm) radiation are significant drivers of decomposition of plant litter in globally important arid and semi-arid ecosystems, such as grasslands and deserts. This occurs through the process of photodegradation, which has implications for nutrient cycling and carbon storage, although considerable uncertainty exists in quantifying its regional and global biogeochemical significance; (3) UV radiation can contribute to climate change via its stimulation of volatile organic compounds from plants, plant litter and soils, although the magnitude, rates and spatial patterns of these emissions remain highly uncertain at present. UV-induced release of carbon from plant litter and soils may also contribute to global warming; and (4) depletion of ozone in the Southern Hemisphere modifies climate directly via effects on seasonal weather patterns (precipitation and wind) and these in turn have been linked to changes in the growth of plants across the Southern Hemisphere. Such research has broadened our understanding of the linkages that exist between the effects of ozone depletion, UV-B radiation and climate change on terrestrial ecosystems.

Effects of solar ultraviolet radiation on terrestrial ecosystems. Patterns, mechanisms, and interactions with climate change.

Ultraviolet radiation (UV) is a minor fraction of the solar spectrum reaching the ground surface. In this assessment we summarize the results of previous work on the effects of the UV-B component (280-315 nm) on terrestrial ecosystems, and draw attention to important knowledge gaps in our understanding of the interactive effects of UV radiation and climate change. We highlight the following points: (i) The effects of UV-B on the growth of terrestrial plants are relatively small and, because the Montreal Protocol has been successful in limiting ozone depletion, the reduction in plant growth caused by increased UV-B radiation in areas affected by ozone decline since 1980 is unlikely to have exceeded 6%. (ii) Solar UV-B radiation has large direct and indirect (plant-mediated) effects on canopy arthropods and microorganisms. Therefore, trophic interactions (herbivory, decomposition) in terrestrial ecosystems appear to be sensitive to variations in UV-B irradiance. (iii) Future variations in UV radiation resulting from changes in climate and land-use may have more important consequences on terrestrial ecosystems than the changes in UV caused by ozone depletion. This is because the resulting changes in UV radiation may affect a greater range of ecosystems, and will not be restricted solely to the UV-B component. (iv) Several ecosystem processes that are not particularly sensitive to UV-B radiation can be strongly affected by UV-A (315-400 nm) radiation. One example is the physical degradation of plant litter. Increased photodegradation (in response to reduced cloudiness or canopy cover) will lead to increased carbon release to the atmosphere via direct and indirect mechanisms.

Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors.

There have been significant advances in our understanding of the effects of UV-B radiation on terrestrial ecosystems, especially in the description of mechanisms of plant response. A further area of highly interesting research emphasizes the importance of indirect UV radiation effects on plants, pathogens, herbivores, soil microbes and ecosystem processes below the surface. Although photosynthesis of higher plants and mosses is seldom affected by enhanced or reduced UV-B radiation in most field studies, effects on growth and morphology (form) of higher plants and mosses are often manifested. This can lead to small reductions in shoot production and changes in the competitive balance of different species. Fungi and bacteria are generally more sensitive to damage by UV-B radiation than are higher plants. However, the species differ in their UV-B radiation sensitivity to damage, some being affected while others may be very tolerant. This can lead to changes in species composition of microbial communities with subsequent influences on processes such as litter decomposition. Changes in plant chemical composition are commonly reported due to UV-B manipulations (either enhancement or attenuation of UV-B in sunlight) and may lead to substantial reductions in consumption of plant tissues by insects. Although sunlight does not penetrate significantly into soils, the biomass and morphology of plant root systems of plants can be modified to a much greater degree than plant shoots. Root mass can exhibit sizeable declines with more UV-B. Also, UV-B-induced changes in soil microbial communities and biomass, as well as altered populations of small invertebrates have been reported and these changes have important implications for mineral nutrient cycling in the soil. Many new developments in understanding the underlying mechanisms mediating plant response to UV-B radiation have emerged. This new information is helpful in understanding common responses of plants to UV-B radiation, such as diminished growth, acclimation responses of plants to UV-B radiation and interactions of plants with consumer organisms such as insects and plant pathogens. The response to UV-B radiation involves both the initial stimulus by solar radiation and transmission of signals within the plants. Resulting changes in gene expression induced by these signals may have elements in common with those elicited by other environmental factors, and generate overlapping functional (including acclimation) responses. Concurrent responses of terrestrial systems to the combination of enhanced UV-B radiation and other global change factors (increased temperature, CO2, available nitrogen and altered precipitation) are less well understood. Studies of individual plant responses to combinations of factors indicate that plant growth can be augmented by higher CO2 levels, yet many of the effects of UV-B radiation are usually not ameliorated by the elevated CO2. UV-B radiation often increases both plant frost tolerance and survival under extreme high temperature conditions. Conversely, extreme temperatures sometimes influence the UV-B radiation sensitivity of plants directly. Plants that endure water deficit stress effectively are also likely to be tolerant of high UV-B flux. Biologically available nitrogen is exceeding historical levels in many regions due to human activities. Studies show that plants well supplied with nitrogen are generally more sensitive to UV-B radiation. Technical issues concerning the use of biological spectral weighting functions (BSWFs) have been further elucidated. The BSWFs, which are multiplication factors assigned to different wavelengths giving an indication of their relative biological effectiveness, are critical to the proper conduct and interpretation of experiments in which organisms are exposed to UV radiation, both in the field and in controlled environment facilities. The characteristics of BSWFs vary considerably among different plant processes, such as growth, DNA damage, oxidative damage and induction of changes in secondary chemicals. Thus, use of a single BSWF for plant or ecosystem response is not appropriate. This brief review emphasizes progress since the previous report toward the understanding of solar ultraviolet radiation effects on terrestrial systems as it relates to ozone column reduction and the interaction of climate change factors.

Impacts of solar ultraviolet-B radiation on terrestrial ecosystems of Tierra del Fuego (southern Argentina). An overview of recent progress.

The southern part of Tierra del Fuego, in the southernmost tip of South America, is covered by dense Nothofagus spp. forests and Sphagnum-dominated peat bogs, which are subjected to the influence of ozone depletion and to increased levels of solar ultraviolet-B radiation (UV-B). Over the last 5 years we have studied some of the biological impacts of solar UV-B on natural ecosystems of this region. We have addressed two general problems: (i) do the fluctuations in UV-B levels under the influence of the Antarctic ozone 'hole' have any measurable biological impact, and (ii) what are the long-term effects of solar (ambient) UV-B on the Tierra del Fuego ecosystems? In this paper, we provide an overview of the progress made during the first 4 years of the project. We highlight and discuss the following results: (1) ambient UV-B has subtle but significant inhibitory effects on the growth of herbaceous and graminoid species of this region (growth reduction < or = 12%), whereas no consistent inhibitory effects could be detected in woody perennials; (2) in the species investigated in greatest detail, Gunnera magellanica, the inhibitory effect of solar UV-B is accompanied by increased levels of DNA damage in leaf tissue, and the DNA damage density in the early spring is clearly correlated with the dose of weighted UV-B measured at ground level; (3) the herbaceous species investigated thus far show little or no acclimation responses to ambient UV-B such as increased sunscreen levels and DNA repair capacity; and (4) ambient UV-B has significant effects on heterotrophic organisms, included marked inhibitory effects on insect herbivory. The results from the experiments summarized in this review clearly indicate that UV-B influences several potentially important processes and ecological interactions in the terrestrial ecosystems of Tierra del Fuego.

Ultraviolet B radiation enhances a phytochrome-B-mediated photomorphogenic response in Arabidopsis.

Ultraviolet B radiation (UV-B, 290-315 nm) can cause damage and induce photomorphogenic responses in plants. The mechanisms that mediate the photomorphogenic effects of UV-B are unclear. In etiolated Arabidopsis seedlings, a daily exposure to 2.5 h of UV-B enhanced the cotyledon opening response induced by a subsequent red light (R) pulse. An R pulse alone, 2.5 h of UV-B terminated with a far-red pulse, or 2.5 h of continuous R caused very little cotyledon opening. The enhancing effect of UV-B increased with fluence rate up to approximately 7.58 micromol m(-2) s(-1); at higher fluence rates the response to UV-B was greatly reduced. The phyA, phyA cry1, and cry1 cry2 mutants behaved like the wild type when exposed to UV-B followed by an R pulse. In contrast, phyB, phyB cry1, and phyB phyA mutants failed to open the cotyledons. Thus, phytochrome B was required for the cotyledon opening response to UV-B --> R treatments, whereas phytochrome A and cryptochromes 1 and 2 were not necessary under the conditions of our experiments. The enhancing effect of low doses of UV-B on cotyledon opening in uvr1 uvr2 and uvr1 uvr3 mutants, deficient in DNA repair, was similar to that found in the wild type, suggesting that this effect of UV-B was not elicited by signals derived from UV-B-induced DNA lesions (cyclobutane pyrimidine dimers and 6-4 photoproducts). We conclude that low doses of UV-B, perceived by a receptor system different from phytochromes, cryptochromes, or DNA, enhance a de-etiolation response that is induced by active phytochrome B.

Functional significance and induction by solar radiation of ultraviolet-absorbing sunscreens in field-grown soybean crops.

Colorless phenylpropanoid derivatives are known to protect plants from ultraviolet (UV) radiation, but their photoregulation and physiological roles under field conditions have not been investigated in detail. Here we describe a fast method to estimate the degree of UV penetration into photosynthetic tissue, which is based on chlorophyll fluorescence imaging. In Arabidopsis this technique clearly separated the UV-hypersensitive transparent testa (tt) tt5 and tt6 mutants from the wild type (WT) and tt3, tt4, and tt7 mutants. In field-grown soybean (Glycine max), we found significant differences in UV penetration among cultivars with different levels of leaf phenolics, and between plants grown under contrasting levels of solar UV-B. The reduction in UV penetration induced by ambient UV-B had direct implications for DNA integrity in the underlying leaf tissue; thus, the number of cyclobutane pyrimidine dimers caused by a short exposure to solar UV-B was much larger in leaves with high UV transmittance than in leaves pretreated with solar UV-B to increase the content phenylpropanoids. Most of the phenylpropanoid response to solar UV in field-grown soybeans was induced by the UV-B component (lambda

Ozone depletion and UVB radiation: impact on plant DNA damage in southern South America.

The primary motivation behind the considerable effort in studying stratospheric ozone depletion is the potential for biological consequences of increased solar UVB (280-315 nm) radiation. Yet, direct links between ozone depletion and biological impacts have been established only for organisms of Antarctic waters under the influence of the ozone "hole;" no direct evidence exists that ozone-related variations in UVB affect ecosystems of temperate latitudes. Indeed, calculations based on laboratory studies with plants suggest that the biological impact of ozone depletion (measured by the formation of cyclobutane pyrimidine dimers in DNA) is likely to be less marked than previously thought, because UVA quanta (315-400 nm) may also cause significant damage, and UVA is unaffected by ozone depletion. Herein, we show that the temperate ecosystems of southern South America have been subjected to increasingly high levels of ozone depletion during the last decade. We found that in the spring of 1997, despite frequent cloud cover, the passages of the ozone hole over Tierra del Fuego (55 degrees S) caused concomitant increases in solar UV and that the enhanced ground-level UV led to significant increases in DNA damage in the native plant Gunnera magellanica. The fluctuations in solar UV explained a large proportion of the variation in DNA damage (up to 68%), particularly when the solar UV was weighted for biological effectiveness according to action spectra that assume a sharp decline in quantum efficiency with increasing wavelength from the UVB into the UVA regions of the spectrum.

Perception of solar UVB radiation by phytophagous insects: behavioral responses and ecosystem implications.

Most of our present knowledge about the impacts of solar UVB radiation on terrestrial ecosystems comes from studies with plants. Recently, the effects of UVB on the growth and survival of consumer species have begun to receive attention, but very little is known about UVB impacts on animal behavior. Here we report that manipulations of the flux of solar UVB received by field-grown soybean crops had large and consistent effects on the density of the thrips (Caliothrips phaseoli, Thysanoptera: Thripidae) populations that invaded the canopies, as well as on the amount of leaf damage caused by the insects. Solar UVB strongly reduced thrips herbivory. Thrips not only preferred leaves from plants that were not exposed to solar UVB over leaves from UVB-exposed plants in laboratory and field choice experiments, but they also appeared to directly sense and avoid exposure to solar UVB. Additional choice experiments showed that soybean leaf consumption by the late-season soybean worm Anticarsia gemmatalis (Lepidoptera: Noctuidae) was much less intense in leaves with even slight symptoms of an early thrips attack than in undamaged leaves. These experiments suggest that phytophagous insects can present direct and indirect behavioral responses to solar UVB. The indirect responses are mediated by changes in the plant host that are induced by UVB and, possibly, by other insects whose behavior is affected by UVB.

Solar Ultraviolet-B Radiation Affects Seedling Emergence, DNA Integrity, Plant Morphology, Growth Rate, and Attractiveness to Herbivore Insects in Datura ferox.

To study functional relationships between the effects of solar ultraviolet-B radiation (UV-B) on different aspects of the physiology of a wild plant, we carried out exclusion experiments in the field with the summer annual Datura ferox L. Solar UV-B incident over Buenos Aires reduced daytime seedling emergence, inhibited stem elongation and leaf expansion, and tended to reduce biomass accumulation during early growth. However, UV-B had no effect on calculated net assimilation rate. Using a monoclonal antibody specific to the cyclobutane-pyrimidine dimer (CPD), we found that plants receiving full sunlight had more CPDs per unit of DNA than plants shielded from solar UV-B, but the positive correlation between UV-B and CPD burden tended to level off at high (near solar) UV-B levels. At our field site, Datura plants were consumed by leaf beetles (Coleoptera), and the proportion of plants attacked by insects declined with the amount of UV-B received during growth. Field experiments showed that plant exposure to solar UV-B reduced the likelihood of leaf beetle attack by one-half. Our results highlight the complexities associated with scaling plant responses to solar UV-B, because they show: (a) a lack of correspondence between UV-B effects on net assimilation rate and whole-plant growth rate, (b) nonlinear UV-B dose-response curves, and (c) UV-B effects of plant attractiveness to natural herbivores.

Signaling among neighboring plants and the development of size inequalities in plant populations.

Transgenic tobacco plants that express an oat phytochrome gene (phyA) under control of the cauliflower mosaic virus (CaMV) 35S promoter and display altered photophysiology were used to test the role of light as a vehicle of information in dominance relationships between neighboring plants. Compared with the isogenic wild type, phyA-overexpressing plants showed dramatically reduced morphological responsivity to changes in the red/far red ratio of the incident light and to the proximity of neighboring plants in spacing experiments. In transgenic canopies an increase in stand density caused the small plants of the population to be rapidly suppressed by their neighbors. In wild-type canopies, plants responded to increased density with large morphological changes, and there appeared to be an inverse relationship between the magnitude of this morphological response and the ranking of the individual plant in the population size hierarchy. In these wild-type populations, size inequality increased only moderately with density within the time frame of the experiments. Our results suggest that, in crowded stands, the ability of individual plants to acquire information about their light environment via phytochrome plays a central role in driving architectural changes that, at the population level, delay the development of size differences between neighbors.

Phytochrome-mediated phototropism in de-etiolated seedlings : occurrence and ecological significance.

Phototropic responses to broadband far red (FR) radiation were investigated in fully de-etiolated seedlings of a long-hypocotyl mutant (lh) of cucumber (Cucumis sativus L.), which is deficient in phytochrome-B, and its near isogenic wild type (WT). Continuous unilateral FR light provided against a background of white light induced negative curvatures (i.e. bending away from the FR light source) in hypocotyls of WT seedlings. This response was fluence-rate dependent and was absent in the lh mutant, even at very high fluence rates of FR. The phototropic effect of FR light on WT seedlings was triggered in the hypocotyls and occurred over a range of fluence rates in which FR was very effective in promoting hypocotyl elongation. FR light had no effect on elongation of lh-mutant hypocotyls. Seedlings grown in the field showed negative phototropic responses to the proximity of neighboring plants that absorbed blue (B) and red light and back-reflected FR radiation. The bending response was significantly larger in WT than in lh seedlings. Responses of WT and lh seedlings to lateral B light were very similar; however, elimination of the lateral B light gradients created by the proximity of plant neighbors abolished the negative curvature only in the case of lh seedlings. More than 40% of the total hypocotyl curvature induced in WT seedlings by the presence of neighboring plants was present after equilibrating the fluence rates of B light received by opposite sides of the hypocotyl. These results suggest that: (a) phytochrome functions as a phototropic sensor in de-etiolated plants, and (b) in patchy canopy environments, young seedlings actively project new leaves into light gaps via stem bending responses elicited by the B-absorbing photoreceptor(s) and phytochrome.

On the opportunity cost of the photosynthate invested in stem elongation reactions mediated by phytochrome.

Seedlings of shade-intolerant species react to alterations of the light climate caused by their neighbors with morphological changes that may influence the pattern of resource acquisition and utilization at the whole-canopy level. One such change, the increased stem elongation rate that is triggered by low red (R, 660 nm) to far-red (FR, 730 nm) ratios (R:FR) in dense canopies, might reduce the amount of assimilates available for leaf area expansion or root growth, and in that way affect resource capture by the canopy. We have tested this hypothesis by comparing the growth of both isolated individuals and canopies of the weed Amaranthus quitensis under conditions differing only in the spectral distribution of the incident light. When canopies received the full spectrum of sunlight, the stems were a large proportion (40-57%) of total biomass. Filtering the FR waveband (and hence raising the R:FR ratio to eliminate the neighbors' proximity-signal) resulted in shorter canopies with lighter stems. However, the growth of leaves and roots was not promoted by this treatment, indicating that the opportunity cost of the assimilates invested in the stems was nil or very small. Filtering the FR had no effect on biomass accumulation when plants were grown as isolated individuals. The higher growth of the canopics under full spectrum could be due to a higher light interception or to a higher efficiency of light conversion into biomass. The first possibility is weakened by the observation that filtering the FR had no effect on the dynamics of soil covering by the crops. The second is indirectly strengthened by results of an experiment with isolated plants showing that stem elongation, stem growth, and total plant biomass can be increased by reducing the flux of R light received by the stems without affecting the light climate of the leaves. Further work is needed to distinguish between these two possibilities; whatever the cause, our results show that the elongation responses to decreased R:FR may lead to a net increase in canopy productivity, and do not necessarily have a negative impact on the growth of resource-harvesting organs.

Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies.

When individual seedlings of Datura ferox and Sinapis alba were transferred to populations formed by plants of similar stature, they responded with an increase in the rate of stem elongation. The reaction was detected within 3 days after transplanting and occurred well before shading among neighbors became important. This rapid response, which may be crucial for success in the competition for light, was reduced or abolished when individual internodes were "blinded" to the far-red radiation scattered by the surrounding seedlings. These results show the operation of a localized, photomorphogenetic control of stem elongation that may play a central role in the plastic adjustment of plants during the early stages of canopy development.