Stephan D. Flint

Effects of increased solar ultraviolet radiation on terrestrial ecosystems

Elevated solar UV-B radiation associated with stratospheric ozone reduction may exert effects on terrestrial ecosystems through actions on plants, microbes, and perhaps on some animals. At the ecosystem level, the effects are less well understood than at the molecular and organismal levels. Many of the most important, yet less predictable, consequences will be indirect effects of elevated UV-B acting through changes in the chemical composition and form of plants and through changes in the abiotic environment. These indirect effects include changes in the susceptibility of plants to attack by insects and pathogens in both agricultural and natural ecosystems; the direction of these changes can result in either a decrease or an increase in susceptibility. Other indirect effects of elevated UV-B include changes in competitive balance of plants and nutrient cycling. The direct UV-B action on plants that results in changes in form or function of plants appears to occur more often through altered gene activity rather than damage. The yield of some crop varieties can be decreased by elevated UV-B, but other varieties are not affected. Plant breeding and genetic engineering efforts should be able to cope with the potential threats to crop productivity due to elevated UV-B. For forest trees, this may be more difficult if effects of elevated UV-B accumulate over several years. All effects of elevated UV-B radiation must be considered in the context of other climate changes such as increased temperature and levels of carbon dioxide, which may alter the UV-B responses, especially for plants. The actions of elevated carbon dioxide and UV-B appear to be largely independent, but interactions occur between changes in UV-B and other factors. Other ecosystem-level consequences of elevated UV-B radiation are emerging and their magnitude and direction will not be easily predicted.

Stratospheric Ozone Reduction, Solar UV-B Radiation and Terrestrial Ecosystems

Stratospheric ozone reduction is occurring and will continue to increase in magnitude into the next century. Yet, the consequences for terrestrial ecosystems of the increased solar UV-B (280–320 nm) radiation resulting from total column ozone reduction are not understood. Based on studies of higher plant response to UV-B, several possible consequences for ecosystems include decreased primary production, altered plant species composition, and altered secondary chemistry with implications for herbivory, litter decomposition and biogeochemical cycles. However, like the assessment of increased atmospheric CO2, extrapolation from studies with isolated plants to ecosystem function is very tenuous at best. Very few UV-B studies have dealt with multispecies systems. Most of the UV-B research in the past two decades (since the first suggestions of ozone reduction) has been conducted as short-term experiments in growth chambers and greenhouses where the unnatural spectral balance of radiation can lead to unrealistic conclusions. Technical difficulties in suitable measurement and manipulation of UV-B radiation also complicate the conduct of reliable experiments. This essay surveys and categorizes some 300 papers from the past 20 years on this subject, draws general conclusions from the research and offers some recommendations with respect to ecosystem consequences.

PLANT PROTECTIVE RESPONSE TO ENHANCED UV-B RADIATION UNDER FIELD CONDITIONS: LEAF OPTICAL PROPERTIES and PHOTOSYNTHESIS

Abstract— Plants of Vicia faba were grown in the field during early to midsummer while receiving two levels of supplemental UV‐B radiation. Light‐saturated photosynthesis and stomatal diffusive conductance of intact leaves did not show any indications of UV‐radiation damage. Supplemental UV treatment did cause increased concentrations of UV‐absorbing flavonoid pigments in leaf tissues and decreased epidermal transmittance of UV radiation. While epidermal transmittance was reduced 30% under the low‐UV treatment, the high‐UV treatment failed to elicit as large a change. However, total amounts of flavonoids in other leaf tissues did increase in response to the high‐UV treatment (up to 12% greater per unit leaf area than for control plants). This may have been a major factor protecting underlying photosynthetic tissues.

Plant Competition for Light Analyzed with a Multispecies Canopy Model. III. Influence of Canopy Structure in Mixtures and Monocultures of Wheat and Wild Oat

SummaryA multispecies canopy photosynthesis simulation model was used to examine the importance of canopy structure in influencing light interception and carbon gain in mixed and pure stands of wheat (Triticum aestivum L.) and wild oat (Avena fatua L.), a common weedy competitor of wheat. In the mixtures, the fraction of the simulated canopy photosynthesis contributed by wheat was found to decline during the growing season and this decline was closely related to reductions in the amount of leaf area in upper canopy layers. For both species in mixture and in monoculture, simulated photosynthesis was greatest in the middle or upper-middle canopy layers and sensitivity analyses revealed that canopy photosynthesis was most sensitive to changes in leaf area and leaf inclination in these layers. Changes in LAI and leaf inclination affected canopy carbon gain differently for mixtures and monocultures, but the responses were not the same for the two species. Results from simulations where the structural characteristics of the two species were substituted indicated that species differences in leaf inclination, sheath area and the fraction of leaf area alive were of minor consequence compared with the differences in total leaf area in influencing relative canopy carbon gain in mixtures. Competition for light in these species mixtures appears to be influenced most by differences in the positioning of leaf area in upper canopy layers which determines, to a great extent, the amount of light intercepted.

Both Solar UVA and UVB Radiation Impair Conidial Culturability and Delay Germination in the Entomopathogenic Fungus Metarhizium anisopliae

The entomopathogenic hyphomycete Metarhizium anisopliae has been used in programs of agricultural pest and disease vector control in several countries. Exposure to simulated solar radiation for a few hours can completely inactivate the conidia of the fungus. In the present study we determined the effect of exposures to full‐spectrum sunlight and to solar ultraviolet A radiation at 320–400 nm (UVA) on the conidial culturability and germination of three M. anisopliae strains. The exposures were performed in July and August 2000 in Logan, UT. The strains showed wide variation in tolerance when exposed to full‐spectrum sunlight as well as to UVA sunlight. Four‐hour exposures to full‐spectrum sunlight reduced the relative culturability by approximately 30% for strain ARSEF 324 and by 100% for strains ARSEF 23 and 2575. The relative UV sensitivity of the two more sensitive strains was different under solar UV from that under ultraviolet B radiation at 280–320 nm (UVB) in the laboratory. Four‐hour exposures to solar UVA reduced the relative culturability by 10% for strain ARSEF 324, 40% for strain ARSEF 23 and 60% for strain ARSEF 2575. Exposures to both full‐spectrum sunlight and UVA sunlight delayed the germination of the surviving conidia of all three strains. These results, in addition to confirming the deleterious effects of UVB, clearly demonstrate the negative effects of UVA sunlight on the survival and germination of M. anisopliae conidia under natural conditions. The negative effects of UVA in sunlight also emphasize that the biological spectral weighting functions for this fungus must not neglect the UVA wavelengths.

Plant Competition for Light Analyzed with a Multispecies Canopy Model. I. Model Development and Influence of Enhanced UV-B Conditions on Photosynthesis in Mixed Wheat and Wild Oat Canopies

SummaryCompetition for light among species in a mixed canopy can be assessed quantitatively by a simulation model which evaluates the importance of different morphological and photosynthetic characteristics of each species. A model was developed that simulates how the foliage of all species attenuate radiation in the canopy and how much radiation is received by foliage of each species. The model can account for different kinds of foliage (leaf blades, stems, etc.) for each species. The photosynthesis and transpiration for sunlit and shaded foliage of each species is also computed for different layers in the canopy. The model is an extension of previously described single-species canopy photosynthesis simulation models. Model predictions of the fraction of foliage sunlit and interception of light by sunlit and shaded foliage for monoculture and mixed canopies of wheat (Triticum aestivum) and wild oat (Avena fatua) in the field compared very well with measured values. The model was used to calculate light interception and canopy photosynthesis for both species of wheat/wild oat mixtures grown under normal solar and enhanced ultraviolet-B (290–320 nm) radiation (UV-B) in a glasshouse experiment with no root competition. In these experiments, measurements showed that the mixtures receiving enhanced UV-B radiation had a greater proportion of the total foliage area composed of wheat compared to mixtures in the control treatments. The difference in species foliage area and its position in the canopy resulted in a calculated increase in the portion of total canopy radiation interception and photosynthesis by wheat. This, in turn, is consistent with greater canopy biomass of wheat reported in canopies irradiated with supplemental UV-B.

PHOTOSYNTHESIS DAMAGE AND PROTECTIVE PIGMENTS IN PLANTS FROM A LA1l11UDINAL ARCTIC/ALPINE GRADIENT EXPOSED TO SUPPLEMENTAL UV-B RADIATION IN THE FIELD

Arctic and alpine plants grown from seed collected from different locations along a latitudinal gradient were studied to determine if populations inhabiting different solar UV-B radiation environments would show differential photosynthetic inhibition under supplemental UV-B irradiation in the field. In general, plants collected from equatorial, alpine sites where solar UV-B irradiance is high, showed no UV-B induced damage of either light-saturated or light-limited photosynthesis, as measured by intact-leaf gas exchange. Photosynthetic inhibition was detected in some but not all ecotypes or species collected from higher latitude locations where effective UV-B irradiance is lower. When exposed to supplemental UV-B irradiation under a full solar spectrum in the field, significant accumulation of UV-absorbing leaf pigments occurred only in populations from higher latitudes. Most alpine populations were apparently protected from UV-B damage without additional pigment accumulation, whereas increased pigment levels did not necessarily act to completely protect populations from higher latitudes. Photosynthesis damage in these species was also not related to leaf weight/leaf area ratios. These results provide additional corroborative evidence for the existence of an appreciable latitudinal gradient in UV-B radiation but suggest that the variation in UV-B sensitivity within and between species cannot be attributed solely to differences in the shielding of UV-B radiation by UV-absorbing leaf pigments and/or leaf structure.

USES OF BIOLOGICAL SPECTRAL WEIGHTING FUNCTIONS AND THE NEED OF SCALING FOR THE OZONE REDUCTION PROBLEM

In several phases of assessing implications of stratospheric ozone reduction for plants, biological spectral weighting functions (BSWF) play a key role: calculating the increase of biologically effective solar ultraviolet-B radiation (UV-BBE) due to ozone reduction, assessing current latitudinal gradients of UV-BBE, and comparing solar UV-BBE with that from lamps and filters in plant experiments. Plant UV action spectra (usually determined with monochromatic radiation in the laboratory with exposure periods on the order of hours) are used as BSWF. Yet, many complicating factors cloud the realism of such spectra for plants growing day after day in polychromatic solar radiation in the field. The uses and sensitivity of BSWF in the stratospheric ozone reduction problem are described. The need for scaling BSWF from action spectra determined with monochromatic radiation in laboratory conditions over periods of hours to polychromatic solar radiation in the field is developed. Bottom-up mechanistic and top-down polychromatic action spectrum development are considered as not satisfactory to resolve realistic BSWF. A compromise intermediate approach is described in which laboratory results are tested under polychromatic radiation in growth chambers and, especially, under field conditions. The challenge of the scaling exercise is to resolve disagreements between expected spectral responses at different scales of time and radiation conditions. Iterative experiments with feedback among the different experimental venues is designed to reduce uncertainties about realistic BSWF in the field. Sensitivity analyses are employed to emphasize characteristics of BSWF that are particularly important in assessing the ozone problem. Implications for use of realistic BSWF both for improved research design and for retrospective analysis of past research is described.

Damage and recovery from UV-B exposure in conidia of the entomopathogens Verticillium lecanii and Aphanocladium album

We evaluated the effects of exposure to doses supplied at an environmentally realistic intensity of UV-B radiation (800 mW m−2 weighted irradiance) on the culturability and germination of selected strains of the entomopathogenic Hyphomycetes Verticillium lecanii and Aphanocladium album. Increased UV-B exposure decreased relative percent culturability for all strains. Four hours of exposure to UV-B were sufficient to reduce the culturability close to zero. The LT50 (50% lethal time) ranged from 120 ± 5 min for the V. lecanii strain ARSEF 6430 to 86 ± 14 min for the A. album strain ARSEF 6433. A strong delay in the germination of surviving conidia was observed. To determine the occurrence of photoreactivation in these two genera, we evaluated the effect of exposure to visible light after exposure to UV-B radiation. There was no significant difference in relative culturability between conidia exposed to visible light after UV-B exposure compared to those incubated in the dark after UV-B exposure. This indicates that photoreactivation, if it occurs, must have limited importance in the repair of the damage induced by UV-B radiation in these two genera.

Effects of UVB Irradiance on Conidia and Germinants of the Entomopathogenic Hyphomycete Metarhizium anisopliae: A Study of Reciprocity and Recovery¶

We tested the effects of irradiances of 920 and 1200 mW m−2 (weighted irradiance) on the conidia and germinants of the entomopathogenic Hyphomycete Metarhizium anisopliae. The conidia were exposed to the two irradiances for 1, 2, 4, 6, 7 or 8 h. Increased exposure decreased relative percent culturability. The inactivation provoked by the irradiance of 1200 mW m−2 was higher than for the 920 mW m−2, with a reduction in the 50% lethal time (LT50) from 6 h 40 min to 4 h 26 min. Reciprocity was not observed when conidia in water suspension and germinants in different stages of the germinative process were exposed to a 17.3 kJ m−2 total dose at both irradiance levels. Although nonreciprocity was observed in all situations, its magnitude varied as a function of metabolic state and/or cell‐cycle phase in which the conidia were at the exposure time. The least difference between the effects of the two irradiance levels was observed when nongerminating conidia in suspension were exposed, and the greatest was observed when conidia were exposed during an advanced germination phase. Doses of 6.6 and 17.3 kJ m−2 supplied through the two irradiance levels delayed the germination of the surviving conidia. At both doses, delay was greater during exposure to the higher irradiance. Nonreciprocity was higher for the 17.3 kJ m−2 dose. Nonreciprocity magnitude, in addition to depending on the conidial physiological state, also depended on dose. The results demonstrate the importance of evaluating the impact of the increase in irradiance during the different stages of the fungal life cycle, especially during the stages which are more sensitive to UV, and not simply in dormant conidia.