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.

Competition for phosphorus: differential uptake from dual-isotope--labeled soil interspaces between shrub and grass.

Two species of Agropyron grass differed strikingly in their capacity to compete for phosphate in soil interspaces shared with a common competitor, the sagebrush Artemisia tridentata. Of the total phosphorus-32 and -33 absorbed by Artemisia, 86 percent was from the interspace shared with Agropyron spicatum and only 14 percent from that shared with Agropyron desertorum. Actively absorbing mycorrhizal roots of Agropyron and Artemisia were present in both interspaces, where competition for the labeled phosphate occurred. The results have important implications about the way in which plants compete for resources below ground in both natural plant communities and agricultural intercropping systems.

Shading and the capture of localized soil nutrients: nutrient contents, carbohydrates, and root uptake kinetics of a perennial tussock grass.

The ability to exploit spatial and temporal heterogeneity in soil resources can be one factor important to the competitive balance of plants. Competition above-ground may limit selective plant responses to below-ground heterogeneity, since mechanisms such as root proliferation and alterations in uptake kinetics are energy-dependent processes. We studied the effect of shading on the ability of the perennial tussock grassAgropyron desertorum to take up nutrients from enriched soil microsites in two consecutive growing seasons. Roots of unshaded plants selectively increased phosphate uptake capacity in enriched soil microsites (mean increases of up to 73%), but shading eliminated this response. There were no changes in ammonium uptake capacity for roots in control and enriched patches for either shaded or unshaded plants. The 9-day shade treatments significantly reduced total nonstructural carbohydrate (TNC) concentrations for roots in 1990, but had no apparent effect on root carbohydrates in 1991 despite dramatic reductions in shoot TNC and fructan concentrations. Enrichment of the soil patches resulted in significantly greater phosphate concentrations in roots of both shaded and unshaded plants, with less dramatic differences for nitrogen and no changes in potassium concentrations. In many respects the shaded plants did surprisingly well, at least in terms of apparent nutrient acquisition. The effects of aboveground competition on nutrient demand, energy requirements, and belowground processes are discussed for plants exploiting soil resource heterogeneity.

The effects of the spatial pattern of defoliation on regrowth of a tussock grass : I. Growth responses.

The effects of the spatial pattern of defoliation within a tussock grass, Agropyron desertorum, were investigated at a semiarid field site. In the middle of the spring growing season (mid-May), tussocks were clipped in repeatable defoliation patterns, and the regrowth of foliage was monitored. These clipping patterns involved removal of foliage from different locations within the tussock, but the total amount of foliage removed was held constant. Active meristems were left intact in all cases. The spatial pattern of defoliation affected both initial rates of tussock regrowth and total growing-season aboveground biomass production. When leaves were removed low in the tussock (older leaves), regrowth was greater than after removal of the same quantity of foliage high in the canopy (younger leaves). These differences in regrowth were due to differences in the rate of new tissue production rather than differences in the timing of senescence. The results were consistent over two years even though aboveground production differed considerably between years. The interaction of the spatial pattern and timing of defoliation was also studied by clipping additional plants in late May. The timing of defoliation affected the relative influence of different defoliation patterns on regrowth. In those defoliation patterns where active meristems were not removed in the late-May clipping, there were no differences in regrowth of tussocks which had either upper or lower foliage removed. However, because the grass culms had elongated by late May, active meristems were higher and were removed by one of the defoliation pattern treatments (a uniform clipping). This resulted in much less regrowth. Differences in the effects of clipping patterns applied in late May were associated with this removal of active meristems. Whereas, differences among clipping treatments following the earlier mid-May defoliation were probably a result of changes in factors which affected tussock carbon gain (e.g., light interception, foliage age structure). In either case, the spatial pattern of defoliation within a tussock grass clearly had significant effects on aboveground regrowth.

The timing and degree of root proliferation in fertile-soil microsites for three cold-desert perennials.

Root proliferation in nutrient-rich soil patches is an important mechanism facilitating nutrient capture by plants. Although the phenomenon of root proliferation is well documented, the specific timing of this proliferation has not been investigated. We studied the timing and degree of root proliferation for three perennial species common to the Great Basin region of North America: a shrub, Artemisia tridentata, a native tussock grass, Agropyron spicatum, and an introduced tussock grass, Agropyron desertorum. One day after we applied nutrient solution to small soil patches, the mean relative growth rate of Agropyron desertorum roots in these soil patches was two to four times greater than for roots of the same plants in soil patches reated with distilled water. Most of the increased root growth came from thin, laterally branching roots within the patches. This rapid and striking root proliferation by Agropyron desertorum occurred in response to N-P-K enrichment as well as to P or N enrichment alone. A less competitive bunchgrass, Agrophyron spicatum, showed no tendency to proliferate roots in enriched soil patches during these two-week experiments. The shrub Artemisia tridentata proliferated roots within one day of initial solution injection in the N-enrichment experiment, but root proliferation of this species was more gradual and less consistent in the N-P-K and P-enrichment experiments, respectively. The ability of Agropyron desertorum to proliferate roots rapidly may partly explain both its general competitive success and its superior ability to exploit soil nutrients compared to Agropyron spicatum in Great Basin rangelands of North America.

The effects of the spatial pattern of defoliation on regrowth of a tussock grass : II. Canopy gas exchange.

The effect of different defoliation, patterns within a tussock grass on CO2 and water vapor exchange of entire tussocks was assessed and compared with differences in regrowth behavior. During rapid spring growth, 60% of the green foliage area was removed from Agropyron desertorum tussocks in different spatial patterns. Compensatory growth responses of defoliated tussocks corresponded well with increases in integrated daytime CO2 exchange rate of tussocks per unit foliage area (CERd) immediately following clipping. When leaves were removed from low in the tussock (older leaves), both regrowth and CERd were greater than after removal of foliage located high in the canopy (younger leaves). Water vapor conductance (gw) increased similarly for all clipped plants, regardless of defoliation pattern. Thus, the differential responses of CERd to the defoliation patterns could not be fully attributed to changes in gw. The increases in gw of all clipped plants resulted in large increses in tussock daytime water loss (Ed) and decreases in tussock water-use efficiency (CERd/Ed), even in the case where mostly older, shaded foliage was removed. Despite increases in CERd, whole-tussock CO2 fixation (net CO2 exchange per tussock) declined immediately after clipping because of the removal of considerable foliage. Whole-tussock CO2 uptake recovered more rapidly in tussocks which had lower leaf blades removed than in tussocks which had upper foliage removed because of differences in the rate of new foliage production.

Hydraulic lift: water efflux from upper roots improves effectiveness of water uptake by deep roots.

Deuterated water absorbed by deep roots of Artemisia tridentata appeared in the stem water of neighboring Agropyron desertorum tussocks. This supports the hypothesis that water absorbed by deep roots in moist soil moves through the roots, is released in the upper soil profile at night, and is stored there until it is resorbed by roots the following day. This phenomenon is termed hydraulic lift. The potential for parasitism of the water stored in the upper soil layers by neighboring plant roots is also shown. The effectiveness of water absorption by deep roots was substantially improved with hydraulic lift as indicated by reductions of 25 to 50% in transpiration on days following experimental circumvention of hydraulic lift. This phenomenon has important implications for plant water relations, mineral nutrient uptake, competitive interactions among neighboring plants and aridland hydrology.

Competitive ability is linked to rates of water extraction : A field study of two aridland tussock grasses.

The relative competitive abilities of Agropyron desertorum and Agropyron spicatum under rangeland conditions were compared using Artemisia tridentata ssp. wyomingensis transplants as indicator plants. We found A. desertorum to have substantially greater competitive ability than A. spicatum as manifested by the responses of Artemisia shrubs that were transplanted into nearly monospecific stands of these grass species. The Artemisia indicator plants had lower survival, growth, reproduction, and late-season water potential in the neighborhoods dominated by A. desertorum than in those dominated by A. spicatum. In similar, essentially monospecific grass stands, neutron probe soil moisture measurements showed that stands of A. desertorum extracted water more rapidly from the soil profile than did those of A. spicatum. These differences in extraction rates correlate clearly with the differences in indicator plant success in the respective grass stands. Nitrogen and phosphorus concentrations in Artemisia tissues suggested these nutrients were not limiting indicator plant growth and survival in the A. desertorum plots.

Hydraulic lift: Substantial nocturnal water transport between soil layers by Artemisia tridentata roots.

Diel soil water potential fluctuations reflected daytime depletion and nocturnal resupply of water in upper soil layers. Transpiration suppression experiments demonstrated that water absorption by roots caused the daytime depletion. The soil water potential data and experimental results suggest that at night water absorbed from moist soil by deeper roots is transported to and lost from roots into drier upper soil layers. The deeper roots appear to absorb and transport water both day and night. Implications for the efficiency of deep roots and water storage, nutrient uptake and water parasitism in upper soil layers are discussed.

Characteristics of successful competitors: an evaluation of potential growth rate in two cold desert tussock grasses.

Within the first few weeks after seedling emergence, Agropyron desertorum, a more competitive tussock grass, had a much higher mean relative growth rate (RGR) than Agropyron spicatum, a very similar, but less competitive species. However, beyond the early seedling stage, the two grasses had a remarkably similar whole-plant RGR in hydroponic culture and aboveground RGR in glasshouse soil, if root temperatures were above approximately 12°C. At soil temperatures between 5 and 12°C, A. desertorum exhibited a 66% greater aboveground RGR than A. spicatum (P<0.05). Both species responded similarly to warming soil temperatures. In the field, however, tiller growth rates were generally similar. Neither species showed marked tiller elongation until a couple of weeks after snowmelt, by which time soil temperatures, at least to a depth of 10 cm, were above 12°C for a significant portion of the day. Aboveground biomass accumulation over a three-year period indicated that both grasses had similar potential growth rates whereas Artemisia tridentata ssp. vaseyana, a common neighbor planted in the same plots, had a much greater potential growth rate. The greater competitive ability of adult A. desertorum, as compared to A. spicatum, cannot be attributed to appreciable differences in potential growth rates.

The effects of the spatial pattern of defoliation on regrowth of a tussock grass : III. Photosynthesis, canopy structure and light interception.

The spatial pattern of foliage removal from a tussock grass can influence regrowth through effects on daily carbon gain (CERd). This field study examined the extent to which tussock photosynthetic responses to different defoliation patterns were associated with changes in whole-canopy attributes (e.g., foliage age structure, canopy light microclimate). During the spring growing season, 60% of the green foliage area was removed from individual Agropyron desertorum tussocks with scissors in different spatial patterns. These patterns represented extremes of defoliation patterns that might be inflicted by natural herbivores. Tussock photosynthesis (per unit foliage area) at high light (2000 µmol photons m-2 s-1 between 400 and 700 nm; P2000) increased following clipping with all defoliation patterns. The increases in P2000 were greater when leaves were removed from low in the tussock (older leaves) than if leaves high in the canopy (younger leaves) were removed. These relative changes of P2000 among clipping patterns paralleled the responses of CERd and regrowth from an earlier study. Furthermore, the changes in P2000 corresponded with increases in the proportion of foliage within the tussocks that was directly illuminated at midday. The greater photosynthesis of tussocks after lower-leaf removal was directly related to a higher proportion of younger foliage and a smaller fraction of foliage shaded within the tussock. In a dense canopy, such as these grass tussocks, the influence of defoliation on whole-canopy attributes may be of primary importance to whole-plant photosynthetic responses.

A test of compensatory photosynthesis in the field: Implications for herbivory tolerance.

The occurrence of compensatory photosynthesis was examined in the field for all foliage elements on two Agropyron bunchgrass species that differ in their evolutionary history of grazing pressure. This is the first reported field study of compensatory photosynthesis in individual foliage elements of graminoids. Compensatory photosynthesis was defined as an increase in the photosynthetic rates of foliage on partially defoliated plants relative to foliage of the same age on undefoliated plants. Compensatory photosynthesis did occur in many individual foliage elements during at least part of their ontogeny. For both species, compensatory photosynthesis was related primarily to delayed leaf senescence and increased soluble protein concentrations, but not to an improvement in the water status of clipped plants. Soluble protein concentration increased in all foliage elements. A delay in senescence on clipped plants was documented for the two oldest, fully-expanded leaves that were present when the plants were initially clipped, but the initiation and senescence of all other foliage elements were not affected by the clipping treatments. Photosynthetic water use efficiency and photosynthetic rates per unit soluble protein of foliage on partially defoliated plants were not increased following the clipping treatments. Although A. desertorum and A. spicatum were exposed to different levels of grazing pressure during their evolutionary history, the phenology, water status, and gas exchange rates of foliage were very similar both for undefoliated as well as partially defoliated plants. Thus, we conclude that compensatory photosynthesis does not appear to be an important ecological component of herbivory tolerance for these species.

Shading reduces exploitation of soil nitrate and phosphate by Agropyron desertorum and Artemisia tridentata from soils with patchy and uniform nutrient distributions.

Shading may both lessen the demand for soil nutrients and also the energy supply for nutrient acquisition. Since root foraging for nutrients in patchy environments can be energy-costly, especially for an immobile nutrient such as phosphate (P), the effects of shading may be most expected in heterogeneous soils. Plant acquisition of nitrate (N) and phosphate from soils with patchy and uniform nutrient distributions was determined in a field study under open sunlight and with shading for two common perennial Great Basin shrub steppe species, Agropyron desertorum and Artemisia tridentata. Partial shading in a pattern which can occur in shrub steppe vegetation significantly decreased plant N and P acquisition from soils both in the patchy and the uniform nutrient treatments. Artemisia was more affected by the shading than was Agropyron. Exploitation of the rather immobile P ion by both species was reduced to a much greater degree by the shading in the patchy distribution treatment than in the uniform nutrient treatment. As expected, plant acquisition of the more mobile N varied little with nutrient distribution treatment for both species and the depression of N acquisition by shading was the same in both nutrient distributions. The effects of shading appeared to have had its primary influence on different components of root foraging in the two species, especially in the nutrient-rich patches. For Agropyron shading primarily affected root proliferation, as indicated by reduced root density in patches. For Artemisia, shading most influenced root physiological uptake capacity and this was most pronounced in the nutrient-rich patches. While aboveground competition for light may generally reduce nutrient acquisition, the effects appear to be most pronounced if root systems of these steppe species are foraging for nutrients such as P in spatially heterogeneous soils.

Belowground productivity of two cool desert communities.

A new technique based upon the dilution of C 14 /C 12 ratios in structural carbon of root systems during the course of the growing season was used to evaluate belowground turnover or productivity of two cool desert communities in northern Utah, USA. This technique provides a measure of turnover of the root system of established perennial plant communities avoiding many of the disadvantages of other techniques. Adjacent communities dominated by Atriplex confertifolia and Ceratoides lanata both exhibited belowground productivity values exceeding aboveground production by three-fold. The greater belowground turnover of the Atriplex-dominated community may be a factor contributing to the maintenance of a greater quantity of aboveground biomass and prolonged periods of active photosynthesis during the driest portions of the year when Ceratoides becomes largely photosynthetically inactive.

Effect of competition on stable carbon isotope ratios of two tussock grass species.

Previous studies have shown that plant carbon isotope composition varies when plants experience differences in water and nutrient availability. However, none have addressed the effect of root interactions, including competition for these soil resources, on carbon isotope ratios. We studied the effect of interspecific root interactions on the productivity and carbon isotope ratios of two Great Basin tussock grass species (Agropyron desertorum and Pseudoroegneria spicata). We compared grasses grown in mixture with sagebrush (Artemisia tridentara) to grasses in similar mixtures but where root interactions with sagebrush were limited by fiberglass partitions. During both years of the study, tussocks growing in competition with sagebrush produced tissue with more negative δ13C values than grasses experiencing limited root interaction with sagebrush. The magnitude of this difference (0.5 to 0.9%) is similar to that found in other studies when soil fertility and moisture availability were altered.

Soil solution phosphate, root uptake kinetics and nutrient acquisition: implications for a patchy soil environment.

The importance of increased root phosphate (P) uptake kinetics, root proliferation and local increases of soil solution P (P1) for P acquisition from fertile soil microsites was explored with a simulation model and calculated uptake was compared with experimental data. Based on the partitioning of added P in microsites to P1 and P adsorbed on soil particles and the results of a dual-isotope-labeling experiment (Caldwell et al. 1991a), acquisition of P from the fertile microsites was some 20 X that of uptake from an equal volume of soil which received only water. Simulations were in general agreement and also showed that elevation of root P uptake kinetics could contribute more to the increased acquisition than did root proliferation under these circumstances. Although increased physiological uptake capacity for P has generally been considered to be of little benefit because of diffusion limitation, in patchy soil environments selective elevation of P uptake kinetics in fertile microsites may be of considerable benefit. These tests were conducted in calcareous soil which releases much less P into the soil solution than do many other soils. In many noncalcareous soils the benefits of selective elevation of root uptake kinetics would likely be greater.

Light field heterogeneity among tussock grasses: Theoretical considerations of light harvesting and seedling establishment in tussocks and uniform tiller distributions.

Although the tussock growth form of caespitose graminoids is widespread, the effect of this growth form on light interception and carbon gain of tillers has received little attention. Daily incident photosynthetic photon flux density (PFDinc) and carbon gain in monospecific stands of tussock grasses were compared with those of a hypothetical distribution with the equivalent tiller density per total ground area, but evenly distributed rather than clumped in tussocks. This was computed for two tussock grasses Pseudoroegneria spicata (Pursh) A. Löve (bluebunch wheatgrass) and Agropyron desertorum (Fisch, ex Link) Schult. (creasted wheatgrass) at different plant densities. Daily PFDinc and net photosynthesis (A) were greater if tillers were distributed uniformly rather than clumped in tussocks, except when the density of tussocks was so great as to approach a uniform canopy. When tussock density per ground area was low, much of the difference between tussock and uniform tiller densities in PFDinc and A was due to shading within the tussocks; up to 50-60% of the potential carbon gain was lost in A. desertorum due to shading within tussocks. In a matrix of tussocks, the light field for establishing seedlings was very heterogeneous; potential A ranged from 7 to 96% relative to an isolated seedling. The mean of daily PFDinc and A for seedlings in a tussock stand were nearly identical to the values in corresponding stands of uniform tiller distributions. It is hypothesized that the loss of A resulting from clumping tillers into tussocks is offset by benefits of protecting sequestered belowground resources from invasion by seedlings of competitors.

Effectiveness of phosphate acquisition by juvenile cold-desert perennials from different patterns of fertile-soil microsites.

Phosphate uptake was measured for Artemisia tridentata, Agropyron desertorum and Pseudoroegneria spicata, three common perennial North American Great Basin species. Four patterns of nutrient-rich microsites were used in the experiments (different distances, densities and nutrient concentrations) All species were more efficient at taking up P from microsites nearest the plants than from more distant microsites. Artemisia and Agropyron acquired P more rapidly from the distant microsites when there was a larger number of microsites and, therefore, a greater probability of encounter. Uptake from the nearest microsites did not increase after 26 days, while uptake from distant microsites increased and was equal to uptake from the nearest microsites by the end of the experiment. Phosphate uptake was four to five times higher for Artemisia than for Agropyron on a shoot mass basis and seven to eight times greater than for Pseudoroegneria, which reflects species relative growth rates. Differences in shoot dry mass were significant among species, but little evidence was found for interspecific competition. Root density, root dry mass and P uptake in the upper part of the soil mixture was higher for Artemisia than the other species. Phosphate acquisition seems to be influenced by the distance of microsites and their density and the ability of plants to encounter and proliferate absorbing organs in the microsites.

A fiber optic point quadrat system for improved accuracy in vegetation sampling.

An automated, fiber optic point quadrat system for vegetation sampling is described. Because the effective point diameter of this system never exceeds 25 µm it minimizes the substantial errors which can arise with conventional point quadrats. Automatic contact detection eliminates operator subjectivity, and permits work in dense canopies. Additionally, sampling speed is increased over that of conventional systems.