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Chapter 4 ECOSYSTEMS AND THEIR COMPONENTS SUMMARY In order to predict the effects of increased levels of W-B on natural and cultivated ecosystems, the nature of the interactions of organisms with environmental vari ables and the adaptations of organisms to changes in nutrients, predation, climate, and light must first be understood. Only then can dose-response relationships for UV-B effects be established. Because these inter actions are complex, mathematical models are often used to express them and to facilitate data handling. The usefulness of these models is limited, however, by the information available. Thus, although data are available on W-B effects on specific organisms and on W -B effects on life cycle stages of organisms, the relationship between the effects on the individual and the effects on the population is not clear. It appears that the yield of food from domestic animals will not significantly decrease even with the most extreme projections of ozone depletion. Economically important cultivated crops may have reduced yields from increased W-B levels. Further assessment is needed of the organismal and cellular properties and adaptations in plants and in most animals that modify the direct and indirect effects of UV-B. Such research must be conducted under carefully simulated field conditions. This capa- bility exists in a number of laboratories; however, a subtropical facility would be valuable. Other food, fiber, and medicinal crops have received relatively little attention and the effects of enhanced UV-B on them cannot be assessed. The potential impacts of increased W-B on natural terrestrial ecosystems have received limited study. Any
63 attempt at the present time to predict potential consequences would be subject to large uncertainties. Nevertheless, several physiological processes of plants (e.g., leaf growth and photosynthesis) have been shown to be adversely affected by W-B. Most of these responses were determined in growth chambers or greenhouses where visible radiation, WV-A, and other environmental factors did not simulate ambient conditions. Since ambient visible radiation and W-A ameliorate most, if not all, of the deleterious effects of UV-B, most of this research needs to be repeated under field conditions for verification. Terrestrial faunal ecosystems have received almost no attention, and nothing can be said of their level of susceptibility. In part, such neglect may be justified because the few available studies indicate that in addi- tion to possessing physiological and biochemical mecha- nisms to alleviate the effects of radiation impinging on the organism, some animals possess behavioral mechanisms that lessen exposure to presumptively damaging radiation. Marine faunal ecosystems have received some attention. Both freshwater and marine systems have been examined in several U.S. laboratories. It is, however, difficult to assess the risk factor of increased W-B directly. In part, the vertical mobility of aquatic creatures and the fact that the dose changes exponentially with depth in the sea make it difficult to measure the received dose as a function of time, although upper and lower bounds can be assigned. No assessment has been made of the con sequences of the qualitative or quantitative changes in a natural aquatic ecosystem exposed to enhanced levels of W-B to determine whether one or more members of that system are particularly sensitive to UV-B. Several aquatic organisms have been exposed to W-B in laboratory situations, and most of these studies have shown dele terious effects on the organisms tested. However, as with plants, the effects appear to be modified by visible light and W-A. The research needs to be repeated under field conditions for verification. If aquatic organisms are generally susceptible to W -B damage in their natural setting, the effects of increased solar W -B could have profound consequences on the stability of the food chains upon which the fish and shellfish used by humans depend. A reduction in primary food organisms (for example, algae) could drastically alter the protein supply for large numbers of people throughout the world and have obvious social and political consequences.
64 INTRODUCTI ON Studies involving several aquatic organisms, insects, and terrestrial plants and animals exposed to various levels of enhanced UV-B have shown a number of detrimental effects on growth, reproduction, and physiological processes. The capacity to tolerate increased levels of UV-B through acclimation or repair of UV-induced damage appears to be limited and is, to some degree, species dependent. The value of most of these studies is in question, however, because they have evaluated UV-B doses either considerably beyond those expected to occur on the basis of currently projected estimates of atmospheric ozone reduction (approximately 7 percent) or under experimental conditions with limited extrapolation potential to natural conditions. The U.S. Environmental Protection Agency is currently supporting limited research programs on both terrestrial crop plants and aquatic organisms, but the preponderance of projects recommended by the NRC (1979a) to help resolve the great uncertainties regarding the biological effects of increased UV radiation have not been implemented. Therefore the uncertainties still exist. EFFECTS ON PLANTS Research Difficulties The inherent complexity of simulating a reasonable representation of enhanced W-B regimes under ambient field conditions has confined research almost exclusively to greenhouses and growth chambers. However, the levels of visible radiation and UV-A are considerably lower under these experimental conditions than under ambient field conditions. Recent evidence strongly suggests that ambient field levels of visible radiation can substan- tially reduce or even negate the damaging effects of UV-B (Sisson and Caldwell 1976, Teramura et al. 1980). Thus extrapolation of research conducted under low visible radiation regimes to effects under field conditions would be tenuous and would undoubtedly overestimate the potentially deleterious effects of enhanced UV-B on plants. Furthermore, the interactive effects of UV-B and other environmental stresses (e.g., water, temperature, air pollutants, and even WV-A) have not been adequately addressed in the context of reduced ozone concentrations
65 Nevertheless, existing evidence suggests that an increase in terrestrial UV-B equivalent to that which would be caused by a 7 percent reduction in atmospheric ozone concentration could be potentially damaging to some higher plants (Biggs and Kossuth 1978). Credible predictions regarding the severity of damage to economically impor tant crop plants or to natural plants are not yet feasi- ble. ~ ~ v ~ ~ ~ ~ ~ & _ ~ - This is even more true with regard to predictions of species displacement or perturbation within the world's natural ecosystems, because there is less information available. Although relatively few plants have been evaluated, a wide range of sensitivity to UV-B radiation has been found in crop plants (Biggs and Kossuth 1978) and agriculturally derived varieties (cultivars) within single species (Krizek 1978). This range of sensitivities may be due in part to the differing capacity or efficiency of plants to repair UV-B damage. Plants also appear to differ in their capacity to attenuate UV-B before it is absorbed by the target molecules. Therefore information is needed regarding repair processes, the limits and rates of acclimation, and whether genetic control for acclimation is already present or must be developed (an evolutionary process) before the question of the effects of increased W-B on plants can be addressed. This information is not currently available. Advances in Knowledge NRC (1979a) addressed the applicable research to 1979 and the limitations of existing light sources for simulating increases in UV-B corresponding to those that would be caused by reduced atmospheric ozone concentrations. Although the Present discussion incorporates the results _ ~ _ _ ~ _ '___ ~ In HA. mean c; n-= of some research cone DelC)L~ 171 7~ O.~vCL11-C~ &~ ~ 1979 are emphasized. Unfortunately, little applicable research has been done since then, because of the research difficulties described above and a lack of funding. The variation among plant species in sensitivity to W-B (Biggs et al. 1975, Biggs and Kossuth 1978, NRC 1979a) may be due, in part, to different acclimation potentials. - An ability to tolerate even ambient W-B levels appears to be induced by concomitant exposure to W. For example, Bogenrieder and Klein (1977 ) found that Rumex alpinus seedlings grown in an environment free of
66 W-B displayed severely depressed photosynthetic rates when exposed to ambient W -B levels. A similar response was found in _. patientia again grown in a W-B-free environment, but then exposed to enhanced levels of W -B under ambient conditions (Sisson and Caldwell 1976). Ambient levels of UV-B even killed some R. alpinus plants after a 3-day exposure period, although all of the R. patientia exposed to enhanced UV-B survived. As discussed by Caldwell (1982), if acclimation to environments with high intensities of UV is a phenotypic response already available to the plant, the anticipated rate of atmos- pheric ozone depletion would not be of concern. If, however, acclimation involves genotypic changes that must occur over a long period of time, the rate of ozone depletion would be of considerable importance. Several studies have recently addressed the question of acclimation by investigating leaf epidermal trans- mittance of UV-B. Wellman (1974) has shown that UV-B- absorbing pigments are synthesized in some species in response to UV levels equivalent to existing ambient fluxes. Leaf epidermal extracts (containing flavonoids and other related pigments) from several plants increased their absorbance at 380 nm after exposure to W-B (Robberecht and Caldwell 1978). Extracts from squash (Cucurbita pepo) leaves exposed to three levels of UV-B increased their absorbance as dose increased (Sisson 1981). Although absorbance by these extracted pigments increased substantially with increasing W-B dose rate, photosynthesis and leaf growth were repressed at the higher radiation level. Even though W-B apparently induced a synthesis of leaf pigments, the attenuation appeared to be insufficient to protect leaf growth processes and the photosynthetic apparatus completely. Nevertheless, this response would be of significant value in alleviating the potentially deleterious effects of any increase in UV-B at the earth's surface. The intensity of biologically effective W-B (NRC 1979a) increases by a factor of more than 7 from the arctic (70°N) to the equator (Caldwell et al. 1980). The increase experienced in moving through this latitudinal gradient greatly exceeds the increase expected from atmospheric ozone reduction at temperate latitudes. The leaf epidermal transmittance of W-B of several plants along this gradient was evaluated by Robberecht et al. (1980). The calculated mean effective UV-B dose transmitted by the epidermis to the physiologically active mesophyll cells was found to be similar along this
67 gradient even though the ambient levels of UV increased substantially. Thus along this latitudinal gradient plants are apparently coping with ambient W through acclimation processes that include a reduction in epidermal transmittance as intensity increases. Whether plants will be able to cope with additional UV-B along this gradient by increasing the attenuation properties of the cuticle, epidermis, or mesophyll cell structure and function is not known. In attempting to evaluate the potential impacts on higher plants, it is important to know whether photo- synthesis and other physiological processes have a reciprocal relationship (i.e., damage is cumulative and dose dependent) with UV-B damage. Reciprocity has been demonstrated in isolated chloroplasts (Jones and Kok 1966) and for photosynthesis in a sensitive plant exposed to UV-B over a 50-day period (Sisson and Caldwell 1977). Trocine et al. (1981) demonstrated that W -B damage is cumulative in two of three seagrasses tested. They suggested that the differential degree of UV-B sensitivity within these species was a function of epidermal cell wall thickness and associated trans- mittance properties. Teramura et al. (1980) demonstrated that reciprocity also applies for photosynthesis in soybeans; the damaging effect of W-B was shown to be more deleterious when visible radiation was low. In these studies, the apparent dependence of response on the total dose rather than on the dose rate suggests that repair of damage within the photosynthetic apparatus may not involve nucleic acid repair systems, which are dose rate dependent (Caldwell 1982). Although the reduction in photosynthesis is less pronounced at high visible radiation levels (Sisson and Caldwell 1976, Teramura et al. 1980), suggesting either photoprotection or photo- repair (see Chapter 3) of the photosynthetic apparatus, the particular repair mechanism(s) involved has not been determined. Caldwell et al. (1980) studied leaf inclination as an avoidance mechanism for reducing the solar W radiation loads on plant leaves. However, at temperate latitudes 40 percent to 75 percent of solar UV-B is in the nondirect sunlight that reaches the leaves, which substantially reduces the effectiveness of leaf inclination as an avoidance mechanism. Their calculations indicated that even vertical foliage received at least 70 percent of the daily effective UV-B. Consequently, a breeding program directed at developing crop plants of economic importance
68 with canopies to avoid direct-beam W radiation may be of little use. Several sites of inhibition within the photosynthetic apparatus have been determined (see review by Caldwell 1982). Inhibition of electron transport associated with photosystem II (Brandle et al. 1977, Yamashita and Butler 1968) disruption of thylakoid membranes and other struc- tural components of the chloroplast (Brandle et al. 1977, Mantai et al. 1970), and inactivation of photosystem I (Okada et al. 1976) have been demonstrated after exposure to UV. Recently, Vu et al. (1981, 1982) demonstrated partial inhibition of carboxylating enzyme activity. Thus UV might be a nearly universal inhibitor of compo- nent reactions within the photosynthetic apparatus, as well as deleterious to its structural integrity. However, these studies were conducted in growth chambers or green- houses with correspondingly low visible radiation levels. In order to predict real-life effects of increases in solar UV, the studies would need to be repeated under ambient conditions where UV-B can be adequately supplemented. Since physiological responses of plants to UV are highly wavelength dependent, an appropriate action spectrum for weighting heterochromatic UV-B becomes necessary for expressing effective dose, determining threshold levels for damage, and developing predictive dose-response relationships. The inconsistency in conclusions that can be arrived at by using different action spectra has been thoroughly addressed elsewhere (Caldwell 1982, NRC 1979a). Although action spectra are useful for a prediction, their utility may be reduced because of apparent synergisms arising from interactions due to different wavelengths (Elkind et al. 1978, Elkind and Han 1978) (see Chapter 3). It is not known whether this synergistic effect is a general phenomenon within plant physiological processes. Attempts to develop new action spectra should therefore incorporate simultaneous investigations into potential synergistic action among the wavelengths involved. This will facilitate accuracy in dose-response relationships and make them more useful in predicting the consequences of increased intensities of UV-B at the earth's surface.
69 EFFECTS ON DOMESTIC ANIMALS Among the domestic animals that are necessary for the maintenance of our food supply, only one breed of cattle appears to show deleterious effects from exposure to solar W. The white-faced Hereford shows some suscepti bility to injury and disease of the eye. Kopecky et al. (1979) have shown that W-B is a probable causal factor in cancer eye (bovine ocular squamous cell carcinoma) and enhances the onset of infectious bovine keratoconjunc- tivitis (IBK), or pinkeye, in these cattle. It is questionable, however, whether the level of injury is serious enough to warrant extensive further investigation. Ladds and Entwistle (1977) reported on squamous cell cancers occurring on the ears and nose of sheep. They found that incidence in tropical Queensland, Australia, was greater than that found in temperate areas in earlier studies (Lloyd 1961). Increasing incidence with advancing age was also demonstrated. The authors suggest that squamous cell cancer in sheep would provide a good model for studies of skin cancer in humans. EFFECTS ON AQUATIC ORGANISMS Research Difficulties Measurement of the effects of enhanced W -B on aquatic organisms presents difficult experimental problems. It is possible and desirable to assess effects of W-B on individual organisms under controlled laboratory condi- tions. These experiments can at least establish which organisms may be sensitive to enhanced UV-B. It is in determining the relationship of the dose received by the organism in the laboratory to that received by the organism in its natural ecosystem that uncertainties occur, because of the many variables in natural systems. First, position of organisms in the water column is conditioned by UV-B, by light other than W -B. by nutrient availability, by the nature of turbulent mixing of the waters by wind, and, in shallower regions, by tidal frictional forces along the bottom. - ~ are seasonal and annual variations in species composi- tions, in larval developmental stages, in predation success, and in the physical transport, turbidity, and pigment-absorptive characteristics of coastal and estuarine waters where major food chain productivity Second, there
70 occurs. The large statistical variance associated with the reproductive success of organisms that produce large numbers of spawn (up to 108 per adult female) makes it difficult to assess the effects of small changes in environmental factors (e.g., a 10 percent change in UV-B levels) with any degree of statistical significance. m is would be particularly difficult without precise base line data regarding the effects of present levels of UV-B. It is important to distinguish between assessing the possible effects of enhanced UV-B on individuals of a species, which can best be accomplished in the laboratory, and assessing the effects of damage to individuals on the populations of those individuals in the natural ecosystem, which requires extensive field studies. Advances in Knowledge The population ecology and dynamics of aquatic food chains--the anchovy, striped bass, herring, shellfish, crustaceans--are just beginning to be studied by interdisciplinary teams of physical hydrographers, phytoplankton-, zooplankton-, and fish-biologists, and biochemists and physiologists. This ecosystem research is expensive because it requires time on board ships and large numbers of personnel. But until the capability is developed for predictions of specific food chain effects under the range of present physical, chemical, and biological interactions, the inclusion of the UV-B variable (unless the effects of UV-B are catastrophic) will not lead to statistically significant conclusions. There is strong experimental evidence that current levels of W-B in surface waters depress near-surface productivity of organisms at the base of food chains (primary productivity) in marine waters (Calkins and Thordardottir 1980, Lorenzen 1979, Smith et al. 1980, Steemann Nielsen 1964). The measurement of the penetra- tion of UV-B below the surface and the estimation of doses to aquatic organisms are very complex. The penetration of UV-B into waters with low transparency has not been as well documented as it has for clear waters (Smith and Baker 1981). Turbidity and blue-light- absorbing material (gelbstoff) in waters that have a high organic matter content severely limit UV-B penetration. This fact, the turbulent mixing of surface waters by wind, the ability of organisms to adjust their positions in the water column, and the 24-hour rhythms of vertical
71 migration observed for many marine species all add to the difficulty of estimating the dose of W-B to which aquatic organisms are exposed. Because of these difficulties, the possible effects of predicted increases in W-B (due to ozone depletion) on phytoplankton populations within the entire photic zone are at present unknown. Attempts have been made to maintain captured phyto- plankton populations in tanks and to document species composition changes and changes in primary productivity resulting from enhanced W-B (Worrest et al. 1978, 198la,b). While these experiments show statistically significant effects of enhanced W -B. the difficulties of mimicking natural mixing conditions, the visible and W-A photic regimes, and the nutrient and predation conditions of the real world make extrapolation of these data to populations in the natural ecosystem difficult. Predic- tion of the effects on food chains for which phytoplankton serve as food sources is even more difficult. These experimental difficulties have not yet been overcome, and, except for the preliminary studies by Worrest et al. (1981a), have not been attempted on any concerted level. Recently, it has been reported (Hunter et al. 1979) that the W -B threshold for lesions and for retardation of growth in anchovy larvae can be reached after exposure during a 4-day period to W-B intensities of 760 joules per square meter (J m~2) (DNA effective dose). These intensities are equivalent to what would be expected at the surface of clear ocean water if stratospheric ozone concentrations were reduced by 25 percent. Current W -B levels just below the sea surface were estimated to be 413 J m~2 over a 4-day period. From Smith and Baker (1979) the absorption coefficient for W-B can be calculated to be approximately 0.2 m~l. This means, for example, that at 5 m below the surface the W -B intensity is reduced to 37 percent of the surface intensity. These data indicate a marginal effect that depends strongly on the vertical distribution of larvae. The particular value of this study is that it attempts to relate in situ measurements of W-B in seawater to physiological effects on a sensitive stage in the life cycle of a commercially important marine species. This physiological study, combined with sampling for the vertical distributions of larvae, physical hydrographic measurements of water mixing patterns, and further measurements of in situ W-B doses, could serve as a model for investigating the effects of W-B on specific food chains in the marine ecosystem. At the least, the
72 research including photoreactivation effects would provide data from which predictions could be made about the significance of enhanced levels of W -B on the anchovy populations. A photorepair mechanism for W -B lesions in anchovy larvae has been reported by Kaupp and Hunter (1981). The amount of light required to activate photorepair mecha- nisms fully was less than 10 percent of that available from the sun on a clear day even in March. Thus the authors concluded that even with increased W-B, sufficient light exists in the sea to ensure photorepair of W damage in anchovy larvae. : it, .. _ ~ ~ · -~ . . . . . . This report again ~''u~ur~eS one a~rr~cu~es Inherent in studying the effects of enhanced W-B in the laboratory where the effects of other wavelength regions of the solar spectrum cannot easily be considered. A number of studies of W effects on aquatic systems (Calkins and Thordardottir 1980, Karanas et al. 1981, Smith and Baker 1980, Smith et al. 1980, Thomson et al. 1980, Worrest et al. 1980) and on underwater penetration and characterization of W (Green and Miller 1975; Green et al. 1980; Smith and Baker 1979, 1981) have been made recently. The phytoplankton studies of Worrest et al. (1978, 1981a,b) and the anchovy and physical optics studies of Hunter et al. (1979) have been used as examples. RESEARCH RECOMMENDATIONS Prediction of the possible effects of increased solar UV-B on economically important biological organisms, such as specific crop species, and on selected ecosystems is not currently possible for two reasons. First, two major areas ot research that may have potential for improving predictive capability and that were proposed bv NRC (1979a) have not been implemented. These are (1) studies AL one elects or ennancea UV-B conducted in the presence of the natural photoperiodic intensities of the complete solar spectrum, and (2) the development of a low-latitude, W-B-transmitting greenhouse facility where specific higher-latitude species of plants or specific aquatic organisms could be subjected to lower-latitude W-B intensities while other conditions such as spectral intensities and temperatures were maintained close to higher-latitude ranges. Second, in the absence of meticulous attention to the need for careful simulation
73 of environmental parameters implicit in the research areas described above, most of the research data reported appear to lack predictive capability. Our assessment therefore is essentially the same as that given in detail in previous reports (NRC 1979a, SRI 1980, 1981), and the research recommendations largely repeat those in the NRC report (1979a). The following list of research recommendations is not exhaustive. It has been limited to those that should receive attention first, but it is not organized according to priority. 1. Most of the current experimental data on plants was gathered under greenhouse or growth chamber conditions where visible light and W-A levels were considerably lower than plants would experience under ambient field conditions. The absence of ambient levels of visible light and W-A appears to increase substantially the susceptibility of plants to damage by the W levels tested. Thus economically important crop plants need to be evaluated in a field situation where enhanced levels of W -B approximating those predicted to occur under reduced atmospheric ozone conditions are simulated. These experimental conditions might best be obtained in a low-latitude (subtropical), minimal-cloud-cover, multiuser facility. Productivity, photobiological, and physiological studies should be conducted simultaneously. During these studies, W levels incident upon plant surfaces should be carefully monitored. Before the data from such a facility could provide the most precise and unequivocal results, it would be necessary to develop instrumentation, data manipulation, and environmental regulating techniques that would enable the facility to simulate the changing ambient conditions of the higher- latitude location whose plants are under study. Without this capability, the data generated would have limited usefulness for predicting the effects of enhanced W-B. Priority should be given to screening for W-B- sensitive species to look for adverse effects on productivity and to study the mechanisms of W -B stress. 2. Sensitive phases of plant growth need to be determined. For example, is the reproductive stage especially sensitive to an increase in W -B? 3. Dose-response curves and threshold levels for reduced crop yields are currently known for few plant species under ambient field conditions. Important crop plants, selected native plants, representative forage
74 plants, and economically and ecologically important forest species need to be similarly evaluated. 4. Virtually nothing is now known about the inter- actions of W and other known stress factors. The interaction of W with such factors as temperature, water stress, and air pollutants needs to be addressed. 5. Studies of the effects of W on aquatic ecosystems must be approached on two levels: (1) the effects on individuals under controlled conditions where all environmental factors are reproduced and W -B levels are varied, and (2) integration of laboratory dose- response data into ecosystem studies to establish possible effects among populations or specific food chains. Only in this way can it be determined whether a reduction in stratospheric ozone concentration will significantly affect aquatic populations. The inter- disciplinary approach used in the Hunter et al. (1979) anchovy study (described earlier) to assess W -B damage to food chains, together with the specific laboratory measurements, should serve as a model for future research proposals.