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The ecological significance of increasing atmospheric carbon dioxide
The ecological significance of increasing atmospheric carbon dioxide Ute Skiba and Malcolm Cresser This article discusses the impact on the plant-soil-water ecosystem of the doubling of atmospheric carbon dioxide (CO,) postulated for the next few decades. In controlled environments, like greenhouses and managed soils, increasing CO2 levels will significantly increase crop yields. In relatively unmanaged environments, such as forests and moorlands, increases in CO2 may cause long-term problems still needing investigation. Nutrient deficiencies in soils and the acidification of soils and freshwaters may occur, as well as the better known climatic change effects.
The carbon dioxide (CO*) concentration of the global atmosphere has been increasing steadily since the beginning of the Industrial Revolution. Conclusive evidence for this comes from analysing air trapped in polar ice cores. When ice into snow is transformed atmospheric-air, which is trapped in the inter-grain spaces,becomes progressively isolated from the surrounding atmosphere. By analysing the air extracted from these bubbles, it is possible to determine the atmospheric CO* content at the time the air was trapped. Such analyses showed that pre-industrial CO* concentrations ranged between 250-290 ~1 I-’ [l], and rose to 345,ul I-’ by 1984 [2]. The percentage change with time is shown in figure 1. At present, atmospheric CO2 concentrations are increasing at a rate of cu. 1.4~1 l-’ [3]. If this increase continues, a doubling of the present CO;! concentration can be expected by the middle of the next century (to 66opll-9.
Ute Skiba, B.Sc., Ph.D. Graduated in microbioloov and comoleted a doctorate in soil microbioib;gy at the University of Sheffield. She is now a research fellow in Soil Science at the University of Aberdeen, working on the anthropogenic and natural processes effecting cation mobility in upland catchment ecosystems. She is particularly interested in the effects of atmospheric pollutants, including CO?. Malcolm C.Chem.
Cresser,
Ph.D.,
A.R.C.S.,
F.R.S.C.,
Graduated in analytical chemistry at Imperial Colleae. London. and comoleted a Ph.D. there in analy&al spectiometry. After a period in the USA he moved to the University of Aberdeen, where he is currently Reader in Soil Science. His interests include environmental and spectrochemical analysis,soil chemistryandfertility; and the impact of atmospheric pollution upon soils and freshwaters.
Endeavour. New Series, Volume 12, No. 3, 1988. 016&9327/88 $3.00 + .OO. 0 1988. Pergamon Press pk. Printed in Great Britain.
CO2 sources and sinks
The primary cause of the current rise in COZ concentration is the combustion of fossil fuels. Between 5 and 6 X 10” tons of fossil carbon is released into the atmosphere every year. Although this would be enough to increase the atmospheric CO* concentration by 2.33~1 I-’ Y-‘; a large percentage of the released CO;?is fixed again. The oceans and forests are the major sinks for CO*. Gaseous CO2 is fixed into organic forms by photosynthetic organisms (higher plants, algae, and some bacteria). Photosynthesis can be summarized by the following simple equation: nCOz + nHZO + light + (CHZO), + n02 + energy A rapidly growing rain forest can fix annually between 1 and 2 kg carbon m-‘. In moderate climates forests and cultivated fields fix between 0.2 and 0.4 kg m-* each year, whereas in the arctic tundra and in deserts as little as 0.01 kg/m-* may be fixed. The most productive CO* sinks on land, the tropical rain forests are, however, disappearing at an alarming rate. Land vegetation and phytoplankton in the oceans fix similar amounts of CO*. The role of marine biota as a major sink of CO2 has been underestimated for some time, as the primary productivity (the fixation of CO2 by photosynthetic organisms) in the open oceans is nutrient limited. On the continental shelfs, however, enough nutrients are available to support substantial phytoplanktonic growth and therefore to provide important sinks for atmospheric CO*. Even on the relatively nutrient-rich continental shelfs the primary factor in determining the amount of CO;! fixed is the limiting availability of other necessary growth substances, such as N, P, and trace elements.
effect of increasing atmospheric CO2 is by far climatic change. CO*, together with various other gases like methane, chlorofluorocarbons, nitrogen oxides, and water vapour trap terrestrial infrared radiation by absorption (the ‘greenhouse effect’), and an increase in these will increase the global atmospheric and surface temperature. As the temperature increases, the water vapour capacity of the atmosphere will rise and further enhance the greenhouse effect. Sophisticated models have been developed to predict climatic changes likely to occur with the increase in the atmospheric CO1 concentration. With a doubling of the present CO* concentration, the mean global surface temperature can be expected to rise by 3.5 to 4.2”C [4]. Warming of the atmosphere will be more severe in winter and in mid to high latitudes. Polar regions may increase by up to 6°C and equatorial regions by less than 1°C [5]. Along with the temperature shift the precipitation pattern, atmospheric moisture content, and cloudiness will probably change as well. It also has been predicted that increases in atmospheric CO2 (and trace gases) could lead to increased summer dryness of the land surface in northern middle and high latitudes, which could lead to serious consequencesfor agriculture [6]. Climate change and water chemistry
Areas which are already wet but will receive in future even heavier precipitation, may experience changes in the way water moves through soil; this could lead to adverse changes in water chemistry. These could occur, for example, as a result of increased snowmelt or greater incidence of surface runoff over acid surface soils. Climatic changes may lead to accelerated accumulation of organic matter, which could lead to soil acidificaClimatic response tion as discussed later. Such changes The most widely considered possible could contribute to serious freshwater 143
Figure 1 increase in atmospheric CO* concentrations from 1750 (280~ I I-’ CO,) to 1970 (340~1 1-l COz) based upon ice-core extraction data from Neftel eta/. [Il.
water acidification in susceptible regions. Increased preicipitation could also lead to increased flooding and soil erosion in some areas, leading again to hydrological and water chemistry changes. Plants and CO2
Of particular interest is the way in which plants are likely to be affected by a doubling in CO2 concentration. Gaseous pollutant effects may be investigated in small growth chambers, or by use of glasshouses containing continuously replaced atmospheres with the desired composition. Figure 2, for example, shows the system used by Mansfield and colleagues at the University of Lancaster in England. Plants which are COZlimited for photosynthesis almost always respond positively to increased atmospheric CO2 concentrations, as shown in figure 3. Photosynthesis is the key to plant growth and there is a direct relationship between photosynthetic rate and growth rate in plants. Most plants fall into one of two groups, according to their response to increased atmospheric COZ levels [8]. Plants which exhibit the
Figure 2
Controlled
atmosphere
C3 pathway of CO2 fixation (the 1st step of photosynthesis is the fixation of CO2 by ribulosebiphosphate to form 2 molecules of phosphoglyceric acid, a 3carbon compound, hence we talk of C3 plants) are very sensitive to elevated CO2 concentrations. In these plans net photosynthesis increases proportionally with increased atmospheric CO:, levels at least up to 680 ~1 1-l. Most plant speciesindigenous to temperate climates belong to the C3 group. Another common group of plants, C4 plants (CO2 is fixed by phosphoenolpyruvate to form oxaloacetate, a 4-carbon compound), are relatively insensitive to increases in atmospheric CO* concentrations. C4 plants (maize, sorghum; plants from hot, tropical, or sunny climates) concentrate CO* before utilizing it. Within the cells of these plants the CO2 concentration is always much greater than the ambient atmospheric concentration. At low atmospheric CO2 concentrations C4 plants are, therefore, more efficient than C3 plants. Growth
yields
The increased growth of C3 plants with elevated CO* concentrations has been successfully exploited by the horticultural industry. Research on COZ enrichment of greenhouse crops is very extensive [9, lo] and the optimal CO2 concentrations for most greenhouse crops are known. The increase in growth yield is greatest with CO* concentrations below 1000,~11-~for all categories of commercial crops - apart from cotton, which seems to benefit much more from CO* enrichment than other species. It should be stressed, however, that these increased growth yields are invariably obtained using highly fertile soils, where
glasshouses
at the University
of Lancaster.
CO,Concentration
lpi I-‘)
Figure 3 The relationship between photosynthetic rate of fopulus dekoides and atmospheric CO2 concentration, after Regehret a/. [7].
no plant nutrient element is likely to become growth-limiting. It has been calculated that doubling in atmospheric CO2 concentration may lead to an increase in crop yields of around 33 per cent [l I]. Yield increases from some individual crop types are shown in Table 1. These increases suggest a dramatic rise in agricultural productivity provided climatic conditions are favourable and nutrients are not limited. Young plants tend to respond more to a doubling in CO* concentration than do old plants. On first exposure to an elevated CO2 concentration the net CO2 exchange rate of many crops increased by 52 per cent, but once these plants had acclimatized to the new concentration, the yield increases were only 29 per cent [ 131.The growth response of C4 plants to increased CO2 concentrations is likely to be only about 25 per cent of that of C3 plants [14]. The response of agricultural crops to elevated CO2 concentrations has been well researched. Information on the effect of elevated CO* concentrations on trees, however, is much less complete. Data are available for seedlings and young trees subjected to varied CO2 concentrations for a few weeks or a few months. Dry weight, stem diameter, and height were increased in most young trees and seedlings [lS], indicating that, at least in the early growth stages, trees respond to elevated CO* concentrations in much the same way that crops do. Some attempts have also been made to look at the response of mature trees to elevated atmospheric CO2 concentrations, by enclosing ends of branches in an atmosphere of elevated CO* concentration at controlled temperature and measuring the rate of photosynthesis. These studies tell us only how elevated atmospheric CO2 concentrations affect the trees over relatively short periods. For trees, long term CO;! effects may in practice be of great importance. As far as the authors are aware, no such studies have been published as yet. The only
TABLE 1 PREDlCTED CROP YlELD INCREASES FROM DOUBLING ATMOSPHERIC CO2 CONCENTRATIONS TO 660 pl I-’ (121 Plant cotton Fruit Grain Leaf Legume seed Root crops Herbaceous Woody
% increase 118 31 31 25 31
49 34 26
evidence that increased atmospheric CO? levels enhanced the growth of trees over long periods comes from a study by La Marche et (11. [16]. The widths of annual rings of bristlecone and limber pine trees at two high-altitude sites in New Mexico and Colorado were increased by 106 per cent in the decade ending in 1983, compared to growth over the years 1850 to 1859, at one site and by 73 per cent at another. It was suggested that this increase in tree growth since the mid-1Yth century could be correlated with increasing concentration of CO? in the atmosphere. Possible other beneficial effects, for example, enhanced frost hardiness, changes in tree physiology, protection from pollutants etc., as a result of increasing atmospheric CO? levels should also be considered in the interpretation of such results. A rise in atmospheric CO? concentrations cointided with an increase in other air pollutants. The increase in tree-ring width could also be partly due, for example, to a fertilizer effect of N or S inputs from the atmosphere. CO2 and stomata1 conductance Stomata are openings on the leaf surfaces which regulate the uptake and release of gases and water vapour. Stomata of most species open in the light and close in the dark. Stomata also tend to open if the CO? concentration in the substomatal cavities’falls below a critical level: this is. presumably, a mechanism to ensure adequate supplies for CO2 fixation [17]. At high atmospheric CO2 concentrations, however, the stomata1 aperture decreases. Generally. the stomatal response of C4 plants to elevated CO2 concentrations is greater than that of C3 plants [ 181. Partial stomata1 closure due to high atmospheric CO? concentrations may have several advantages for the plant. These are discussed briefly below.
B. A. Kimball and S. B. Idso [19] found that a decrease in stomata1 aperture as a result of elevated CO? levels reduced the transpiration rate of water by 34 per cent. Contrary to this, plants grown in high CO1 atmospheres tend to have, in the longer term, larger leaf surface areas, so that leaf transpiration would be expected to increase. Research, however, has shown that generally the beneficial effects of increased water-use efficiency prevail. As long as water stress is not too great, CO-, enrichment will stimulate growth of water-stressed plants as much as it stimulates that of well-watered plants [20.21]. In C4 plants increased crop yields with elevated CO, concentrations seem to be primarily due to smaller stomata1 apertures and increased water-use efficiency. An increase in the efficiency of plant use of water could influence drainage water amount and chemistry, and. in the longer term, soil chemistry. Air pollution damage reduction Stomata are the main route of entry of gaseous air pollutants into leaves. As stomata1 conductance is reduced at elevated CO, concentrations, it is logical to suppose that CO2 could protect plants from air pollution, or at least reduce the extent of damage [22]. The atmospheric pollutants of concern are sulphur dioxide (SO,), oxidesof nitrogen (NO,), and ozone (0,). In European countries burning of fossil fuel is the main source of gaseous SO2 and motorized vehicles are the main source of NO,. High levels of NO, contribute to increased Oi levels. These gaseous pollutants can cause injury to plants, and reduce their growth. Elevated SO?, 03, and NO, are widely believed to play a major role in the forest dieback observed in central Europe [23]. In some plants. fumigation with SO, or O3 alone caused increased stomata1 opening [24. 251. At high CO1 concentrations. however, stomata1 conductante is reduced and this allows less gaseous pollutants to enter. R. W. Carlson [26] showed that a reduction in
I $ ” ‘\ E > ‘I. “, *’ E “\.\. .Y iE 10 $ $$ f 0I_ 0.0 0.2
, ‘-1.
.450 )III-’ co, \ 0.4
l -. 0.6
SO, Concentration
Water use eficiency The stomata1 response to elevated CO2 concentrations is important in terms of crop productivity, as the efficiency of the plants to use water is greatly increased.
mo cl I-’ co,
0.8
3oo)rllr’
photosynthesis in soya bean, as a response to high SO? levels, was much less in the presence of high levels of CO2 (figure 4). L-Y. Hou et al. [27] showed that high CO.-?concentrations could decrease SO?, Injury to alfalfa and also reduce the Inhibition of photosynthesis caused by SOZ and NO1 mixtures. Ozone leaf injury in the presence of about 800~ I I-’ CO? was reduced by 14 per cent for pinto bean and by 66 per cent for tobacco [28]. Plant-plant interactions Not all plants respond in the same way to elevated CO? concentrations. Doubling of the ambient CO2 levels could have a significant effect on the species distribution. As C3 plants generally benefit more from elevated CO7 concentrations, these will tend to outgrow C4 competitors. For example, in one experiment increasing the atmospheric CO> concentration from 350 to 600 or IO00 ~1 I-~I increased the growth of the C3 weed, velvet leaf (Abutilon theophrust: Medic) relative to the C4 crop, corn [14). A C3 crop would, however, compete more successfully with C4 weeds at elevated CO2 concentrations. Also among C3 plant communities, differences in response to high atmospheric CO? levels lead to one species being a superior competitor. A I : 1 mixture of ryegrass and white clover was sown at ambient and elevated CO? levels (275 and 547~1 1-l CO?). At low CO1 levels ryegrass was clearly the superior competitor, whereas at high CO1 levels clover in the mixture dominated [291. Changes in branching, flowering, fruit and seed production, seed quality, and flower abortion were also observed with elevated levels of atmospheric CO?. Enhanced branching and tillering in high CO? atmospheres has been reported for barley, rice, wheat, soya bean, pea, and rose. Increased branching enables plants to exploit available space better and increases the number of potential flowering and fruiting sites [30]. In a few garden plants. time to flowering and time to maximum floral display was reduced with increasing CO?, [3 I]. The effect of CO7 on flowering IS at least species specific, if not genotype specific. A doubling in flowering by one species without concomitant increase in other insect-pollinated species in that community. could drastically effect pollinator attraction. to the detriment and eventual loss of some species.
co,
1.0
(cl I-‘1
Figure 4 The effect of SO? on photosynthesis of varying COP concentrations for Glycine max. L. after Carlson 1261.
Nutrient availability Plants grown at elevated CO, levels develop more vigorous root systems, which can exploit a larger area of soil for water and plant nutrients. With higher growth yields correspondingly gr;eater amounts of nutrient elements must be 145
E 2
1.3
;
1.2
5 ‘E
1.1
TABLE
2 EFFECT OF HIGH SOIL ATMOSPHERE CO2 CONCENTRATION ON THE MOBILIZATION OF SELECTED CATIONIC SPECIES FROM A GARDEN SOIL
Soil atmosphere
Ca
Solute component,pg K Mg
ml-’ Na
Al
s .h 3 0) a
3% co2 Normal air
1.0 0.9 440
540
640
CO2 Concentration
740
840
CO2 and the soil environment
The CO* concentration in the soil atmosphere tends to be 10 to 100 times greater than that in the above-ground atmosphere because of continued generation of COz by biological processes (mainly
1987
ONDJF
M
A
1988
Figure 6 Seasonal variations in soil atmospheric COP concentrations at 300 mm depth for an upland moor in north-east Scotland.
146
0.47 0.34
0.35 0.27
0.11 0.09
940
absorbed through the roots. R. J. Luxmoore et al. [32] showed that one-yearold pine seedlings took up more N and other plant nutrients from the soil at elevated CO2 concentrations (figure 5). Their results also showed that, at particularly high levels of COz, P and K were used more efficiently and less P, K, and NO3 were leached from soil. For plants grown at elevated CO2 concentrations for long periods, however, one can envisage an eventual decrease in nutrients available in the soil. Nutrient deficiencies cause stress in plants, decrease the yield, and possibly change the frost hardiness, which could also make them more vulnerable to insect attacks and viral infections. It cannot, therefore, be ruled out that rising atmospheric CO2 concentrations have contributed to forest dieback observed in Central Europe. If CO2 is a contributing factor, diverse symptoms might be anticipated at different sites. Although the rising CO* concentrations in this casewould be beneficial in protecting the forests from SO2 and 0s injuries, faster growth could lead to nutrient deficiencies and soil acidification on susceptible soils. The latter could, in turn, lead to freshwater acidification.
S
0.41 0.27
(pl I-‘)
Figure 5 Effect of atmospheric CO2 concentration on Ca, N, Mg, and P in Virginia Pine seedlings, extracted from data of Luxmooreet a/. 1321. Contents are relative to amounts at 340~1 I-’ CO*.
A
0.15 0.11
M
root and microbial respiration). In upland moorland soils in the north-east of Scotland, soil atmospheric CO?, levels between 1 and 2 per cent (10000-20000 ~1 1-l CO*) are not unusual (Skiba and Cresser, unpublished results, figure 6). Soil CO2 concentrations vary with temperature and moisture content of the soil. Highest concentrations are usually recorded in the summer months. Elevated atmospheric CO2 concentrations increase plant growth, which also results in development of more vigorous roots. Microbial populations are stimulated in the vicinity of plant roots (the rhizosphere) as a result of the release of organic substances from the roots and the decay of old root cells. With more vigorous root systems, the surface area of the rhizosphere increases and more root-derived substances are released. Bigger plants will also produce more litter and other plant debris. Overall it can be expected that the amounts of organic substances added to the soil will be increased. Indirectly, elevated atmospheric CO2 concentrations, therefore, should enhance biological activity in the soil. Under aerobic conditions this means an increased consumption of 02 with subsequent release of COz. A large proportion of the soil CO* will diffuse to the surface and then into the atmosphere. It can be expected that an even further substantial increase in atmospheric CO* may result from increased soil respiration. As postulated above, faster growth may deplete nutrients in the soil. On the other hand, stimulated microbial activity in the soil may turn over the organic matter at a quicker rate; that is, may release more nutrients for plant growth. Most plant nutrients, however, are available for both plants and microorganisms, so that significant amounts may be temporarily immobilized as microbial biomass. Increasing the input of organic matter into soil may accelerate the acidification of the soil, especially if base cation supply is limited and litter accumulation increases. Enhanced uptake of cations by faster growing plants will have the same effect. The present authors have shown that when a garden soil was equilibrated with a high concentration of CO* (3 per cent) by flushing with an appropriate gas mixture, and subsequently leached with rainwater, more
cations were leached from the soils treated with 3 per cent CO2 than with air (Table 2, Skiba and Cresser, unpublished results). This process also could accelerate the development of nutrient deficiencies and soil acidification. It appears, therefore, that elevated atmospheric CO* concentrations could well have adverse effects on the soil environment in the long term. On managed land, soil acidification and nutrient deficiences can be alleviated by fertilization. Large forested areas and upland moorland sites could be expected to suffer, however. Much more research is needed to show conclusively long-term effects of elevated atmospheric CO* concentrations on soil/plant interactions.
Conclusion
Much of what has been said so far is factual, but some is, of necessity, speculative. We have not considered possible implications of plant physiological changes which might be induced by increased CO2 in terms of food quality for higher organisms, from insects through to man. This is deliberate, because so little is known. Thus, if a single conclusion is to be reached, it must be that there is a vital and urgent need for research on potential ecological effects on a broad front. Climatic change modellers have led the way, but they could be studying the tip of a potentially very damaging iceberg.
Acknowledgements
The authors are indebted to the DOE (UK) and NERC for financial support and to Sarah Woodin for figure 2.
References
[l] Neftel, A., Moor, E., Oeschger,H. and Stauffer, B., Nature, Lond. 315, 45, 1985.
[2] Gammon,R. H., Sundquist,E. T. and Fraser, P. J., in ‘Atmospheric Carbon Dioxide and the Global Carbon Cycle’, Trabalka, J. R. (ed.), US DOE/ER0239,Nat. Tech. Inform. Service,1985.
131 Prudhomme, T. I., Oechel, W. C., Hastings, S. J. and Lawrence, W. T., in ‘The Potential Effects of Carbon Dioxide Induced Climatic Changes in Alaska’, McBeath, J. H. (ed.), University of Alaska Fairbanks 99701, 1984. 141 Schlesineer. M. E. and Mitchell. J. F. ’ ’ B., in ‘P;bjdcting the Climatic Effects of Increasing Carbon Dioxide’, MacCracken, M. C. and Luther, F. M. (eds), US DOE/ER-0237, Nat. Tech. Infor. Service, 1985. [5] Gates, D. M., in ‘CO2 and Plants’, Lemon. E. R. (ed.). A.A.A.S. Selected Symposium 84: Washington, 1983. [6] Mitchell, J. F. B. and Warrilow, D. A., Nature, Lond. 330, 238, 1987. [7] Regehr, D. L., Bazzaz, F. A. and Boggers, W. R., Photosynthetica9,52,1975. [8] Fitter, A. H. and Hay, R. K. M. (eds), ‘Environmental Physiology of Plants’, Academic Press, London, 1983. [9] Enoch, H. Z. and Kimball, B. A. (eds), ‘Carbon Dioxide Enrichment of Greenhouse Crops’, C.R.C. Press, Florida, 1986. [lo] Lemon, E. R. (ed.), ‘CO2 and Plants’, A.A.A.S. Selected Symposium, Washington, 1983.
Kimball, B. A., Agron. J. 75,779, 1983. [::IEnrichment Kimball, B. A., in ‘Carbon Dioxide of Greenhouse Crops’,
(231 Landholt, W. and Keller, T., Experientia 41, 301, 1985. [24] Majernik, 0. and Mansfield, T. A., Enoch, H. Z. and Kimball, B. A. (eds), Nature, Lond. 227, 371, 1970. C.R.C. Press, Florida, 1986. [25] Schertz, R. D., Kender, W. J. and Musselman, R. C., Sci. Hortic. 13, 37, 1131Cure, J. D. and Acock, B., Agri. Forest Met. 8, 127, 1986. 1980. [14JPatterson, D. T. and Flint, E. P., Weed [26] Carlson, R. W., Environ. Poll. (A) 30, Sci. 28,71, 1980. 309, 1983. [15] Sionit, N. and Kramer, P. J., in ‘Carbon [27] Hou, L-Y., Clyde Hill, A. and SoleimaDioxide Enrichment of Greenhouse ni, A., Environ. Poll. (A) 12, 7, 1977. Crops’, Enoch, H. Z. and Kimball, B. [28] Heck, W. W. and Dunning, J. A., A. (eds). C.R.C. Press. Florida, 1986. APEA J. 17, 112, 1967. [16] La ‘Marche, V. C. Jr., Graybill, D. A., [29] Overdiek, D., Unpublished results cited Fritts, H. C. and Rose, M. R., Science by Strain, B. R. and Bazzaz, F. A., in 225, 1019, 1984. ‘CO2 and Plants’, Lemon, E. R. (ed), [17] Raschke, K., Ann. Rev. PI. Physiol. 26, A.A.A.S. Selected Symposium, 309, 1975. Washington, 1983. [18] Rogers, H. H., Bingham, G. E., Cure, [30] Acock, B. and Pasternak, D., in ‘CarJ.D.,Smith,J.M.andSurano,K.A.,J. bon Dioxide Enrichment of Greenhouse Environ. Qual. 12,569, 1983. Crops’, Enoch, H. Z. and Kimball, B. [19] Kimball, B. A. and Idso, S. B., Agric. A. (eds), C.R.C. Press, Florida, 1986. Water Manage 7,55, 1983. [31] Garbutt, K. and Bazzaz, F. A., New [20] Gifford, R. M., Amt. J. P/ant Physiol. 6, Phvtol. 98. 433. 1984. 367. 1979. [32] Luxmoore, R. J., O’Neill, E. G., Ells, J. [21] Sionit, N., Hellmers, A. and Strain, B. M. and Rogers, H. H. J. Environ. Qua/. R.. Crop Sci. 20,687, 1980. 15, 24, 1986. [22] Majernik, 0. and Mansfield, T. A., Environ. Pollut. (A) 3, 1, 1972.
147
The carbon dioxide (CO*) concentration of the global atmosphere has been increasing steadily since the beginning of the Industrial Revolution. Conclusive evidence for this comes from analysing air trapped in polar ice cores. When ice into snow is transformed atmospheric-air, which is trapped in the inter-grain spaces,becomes progressively isolated from the surrounding atmosphere. By analysing the air extracted from these bubbles, it is possible to determine the atmospheric CO* content at the time the air was trapped. Such analyses showed that pre-industrial CO* concentrations ranged between 250-290 ~1 I-’ [l], and rose to 345,ul I-’ by 1984 [2]. The percentage change with time is shown in figure 1. At present, atmospheric CO2 concentrations are increasing at a rate of cu. 1.4~1 l-’ [3]. If this increase continues, a doubling of the present CO;! concentration can be expected by the middle of the next century (to 66opll-9.
Ute Skiba, B.Sc., Ph.D. Graduated in microbioloov and comoleted a doctorate in soil microbioib;gy at the University of Sheffield. She is now a research fellow in Soil Science at the University of Aberdeen, working on the anthropogenic and natural processes effecting cation mobility in upland catchment ecosystems. She is particularly interested in the effects of atmospheric pollutants, including CO?. Malcolm C.Chem.
Cresser,
Ph.D.,
A.R.C.S.,
F.R.S.C.,
Graduated in analytical chemistry at Imperial Colleae. London. and comoleted a Ph.D. there in analy&al spectiometry. After a period in the USA he moved to the University of Aberdeen, where he is currently Reader in Soil Science. His interests include environmental and spectrochemical analysis,soil chemistryandfertility; and the impact of atmospheric pollution upon soils and freshwaters.
Endeavour. New Series, Volume 12, No. 3, 1988. 016&9327/88 $3.00 + .OO. 0 1988. Pergamon Press pk. Printed in Great Britain.
CO2 sources and sinks
The primary cause of the current rise in COZ concentration is the combustion of fossil fuels. Between 5 and 6 X 10” tons of fossil carbon is released into the atmosphere every year. Although this would be enough to increase the atmospheric CO* concentration by 2.33~1 I-’ Y-‘; a large percentage of the released CO;?is fixed again. The oceans and forests are the major sinks for CO*. Gaseous CO2 is fixed into organic forms by photosynthetic organisms (higher plants, algae, and some bacteria). Photosynthesis can be summarized by the following simple equation: nCOz + nHZO + light + (CHZO), + n02 + energy A rapidly growing rain forest can fix annually between 1 and 2 kg carbon m-‘. In moderate climates forests and cultivated fields fix between 0.2 and 0.4 kg m-* each year, whereas in the arctic tundra and in deserts as little as 0.01 kg/m-* may be fixed. The most productive CO* sinks on land, the tropical rain forests are, however, disappearing at an alarming rate. Land vegetation and phytoplankton in the oceans fix similar amounts of CO*. The role of marine biota as a major sink of CO2 has been underestimated for some time, as the primary productivity (the fixation of CO2 by photosynthetic organisms) in the open oceans is nutrient limited. On the continental shelfs, however, enough nutrients are available to support substantial phytoplanktonic growth and therefore to provide important sinks for atmospheric CO*. Even on the relatively nutrient-rich continental shelfs the primary factor in determining the amount of CO;! fixed is the limiting availability of other necessary growth substances, such as N, P, and trace elements.
effect of increasing atmospheric CO2 is by far climatic change. CO*, together with various other gases like methane, chlorofluorocarbons, nitrogen oxides, and water vapour trap terrestrial infrared radiation by absorption (the ‘greenhouse effect’), and an increase in these will increase the global atmospheric and surface temperature. As the temperature increases, the water vapour capacity of the atmosphere will rise and further enhance the greenhouse effect. Sophisticated models have been developed to predict climatic changes likely to occur with the increase in the atmospheric CO1 concentration. With a doubling of the present CO* concentration, the mean global surface temperature can be expected to rise by 3.5 to 4.2”C [4]. Warming of the atmosphere will be more severe in winter and in mid to high latitudes. Polar regions may increase by up to 6°C and equatorial regions by less than 1°C [5]. Along with the temperature shift the precipitation pattern, atmospheric moisture content, and cloudiness will probably change as well. It also has been predicted that increases in atmospheric CO2 (and trace gases) could lead to increased summer dryness of the land surface in northern middle and high latitudes, which could lead to serious consequencesfor agriculture [6]. Climate change and water chemistry
Areas which are already wet but will receive in future even heavier precipitation, may experience changes in the way water moves through soil; this could lead to adverse changes in water chemistry. These could occur, for example, as a result of increased snowmelt or greater incidence of surface runoff over acid surface soils. Climatic changes may lead to accelerated accumulation of organic matter, which could lead to soil acidificaClimatic response tion as discussed later. Such changes The most widely considered possible could contribute to serious freshwater 143
Figure 1 increase in atmospheric CO* concentrations from 1750 (280~ I I-’ CO,) to 1970 (340~1 1-l COz) based upon ice-core extraction data from Neftel eta/. [Il.
water acidification in susceptible regions. Increased preicipitation could also lead to increased flooding and soil erosion in some areas, leading again to hydrological and water chemistry changes. Plants and CO2
Of particular interest is the way in which plants are likely to be affected by a doubling in CO2 concentration. Gaseous pollutant effects may be investigated in small growth chambers, or by use of glasshouses containing continuously replaced atmospheres with the desired composition. Figure 2, for example, shows the system used by Mansfield and colleagues at the University of Lancaster in England. Plants which are COZlimited for photosynthesis almost always respond positively to increased atmospheric CO2 concentrations, as shown in figure 3. Photosynthesis is the key to plant growth and there is a direct relationship between photosynthetic rate and growth rate in plants. Most plants fall into one of two groups, according to their response to increased atmospheric COZ levels [8]. Plants which exhibit the
Figure 2
Controlled
atmosphere
C3 pathway of CO2 fixation (the 1st step of photosynthesis is the fixation of CO2 by ribulosebiphosphate to form 2 molecules of phosphoglyceric acid, a 3carbon compound, hence we talk of C3 plants) are very sensitive to elevated CO2 concentrations. In these plans net photosynthesis increases proportionally with increased atmospheric CO:, levels at least up to 680 ~1 1-l. Most plant speciesindigenous to temperate climates belong to the C3 group. Another common group of plants, C4 plants (CO2 is fixed by phosphoenolpyruvate to form oxaloacetate, a 4-carbon compound), are relatively insensitive to increases in atmospheric CO* concentrations. C4 plants (maize, sorghum; plants from hot, tropical, or sunny climates) concentrate CO* before utilizing it. Within the cells of these plants the CO2 concentration is always much greater than the ambient atmospheric concentration. At low atmospheric CO2 concentrations C4 plants are, therefore, more efficient than C3 plants. Growth
yields
The increased growth of C3 plants with elevated CO* concentrations has been successfully exploited by the horticultural industry. Research on COZ enrichment of greenhouse crops is very extensive [9, lo] and the optimal CO2 concentrations for most greenhouse crops are known. The increase in growth yield is greatest with CO* concentrations below 1000,~11-~for all categories of commercial crops - apart from cotton, which seems to benefit much more from CO* enrichment than other species. It should be stressed, however, that these increased growth yields are invariably obtained using highly fertile soils, where
glasshouses
at the University
of Lancaster.
CO,Concentration
lpi I-‘)
Figure 3 The relationship between photosynthetic rate of fopulus dekoides and atmospheric CO2 concentration, after Regehret a/. [7].
no plant nutrient element is likely to become growth-limiting. It has been calculated that doubling in atmospheric CO2 concentration may lead to an increase in crop yields of around 33 per cent [l I]. Yield increases from some individual crop types are shown in Table 1. These increases suggest a dramatic rise in agricultural productivity provided climatic conditions are favourable and nutrients are not limited. Young plants tend to respond more to a doubling in CO* concentration than do old plants. On first exposure to an elevated CO2 concentration the net CO2 exchange rate of many crops increased by 52 per cent, but once these plants had acclimatized to the new concentration, the yield increases were only 29 per cent [ 131.The growth response of C4 plants to increased CO2 concentrations is likely to be only about 25 per cent of that of C3 plants [14]. The response of agricultural crops to elevated CO2 concentrations has been well researched. Information on the effect of elevated CO* concentrations on trees, however, is much less complete. Data are available for seedlings and young trees subjected to varied CO2 concentrations for a few weeks or a few months. Dry weight, stem diameter, and height were increased in most young trees and seedlings [lS], indicating that, at least in the early growth stages, trees respond to elevated CO* concentrations in much the same way that crops do. Some attempts have also been made to look at the response of mature trees to elevated atmospheric CO2 concentrations, by enclosing ends of branches in an atmosphere of elevated CO* concentration at controlled temperature and measuring the rate of photosynthesis. These studies tell us only how elevated atmospheric CO2 concentrations affect the trees over relatively short periods. For trees, long term CO;! effects may in practice be of great importance. As far as the authors are aware, no such studies have been published as yet. The only
TABLE 1 PREDlCTED CROP YlELD INCREASES FROM DOUBLING ATMOSPHERIC CO2 CONCENTRATIONS TO 660 pl I-’ (121 Plant cotton Fruit Grain Leaf Legume seed Root crops Herbaceous Woody
% increase 118 31 31 25 31
49 34 26
evidence that increased atmospheric CO? levels enhanced the growth of trees over long periods comes from a study by La Marche et (11. [16]. The widths of annual rings of bristlecone and limber pine trees at two high-altitude sites in New Mexico and Colorado were increased by 106 per cent in the decade ending in 1983, compared to growth over the years 1850 to 1859, at one site and by 73 per cent at another. It was suggested that this increase in tree growth since the mid-1Yth century could be correlated with increasing concentration of CO? in the atmosphere. Possible other beneficial effects, for example, enhanced frost hardiness, changes in tree physiology, protection from pollutants etc., as a result of increasing atmospheric CO? levels should also be considered in the interpretation of such results. A rise in atmospheric CO? concentrations cointided with an increase in other air pollutants. The increase in tree-ring width could also be partly due, for example, to a fertilizer effect of N or S inputs from the atmosphere. CO2 and stomata1 conductance Stomata are openings on the leaf surfaces which regulate the uptake and release of gases and water vapour. Stomata of most species open in the light and close in the dark. Stomata also tend to open if the CO? concentration in the substomatal cavities’falls below a critical level: this is. presumably, a mechanism to ensure adequate supplies for CO2 fixation [17]. At high atmospheric CO2 concentrations, however, the stomata1 aperture decreases. Generally. the stomatal response of C4 plants to elevated CO2 concentrations is greater than that of C3 plants [ 181. Partial stomata1 closure due to high atmospheric CO? concentrations may have several advantages for the plant. These are discussed briefly below.
B. A. Kimball and S. B. Idso [19] found that a decrease in stomata1 aperture as a result of elevated CO? levels reduced the transpiration rate of water by 34 per cent. Contrary to this, plants grown in high CO1 atmospheres tend to have, in the longer term, larger leaf surface areas, so that leaf transpiration would be expected to increase. Research, however, has shown that generally the beneficial effects of increased water-use efficiency prevail. As long as water stress is not too great, CO-, enrichment will stimulate growth of water-stressed plants as much as it stimulates that of well-watered plants [20.21]. In C4 plants increased crop yields with elevated CO, concentrations seem to be primarily due to smaller stomata1 apertures and increased water-use efficiency. An increase in the efficiency of plant use of water could influence drainage water amount and chemistry, and. in the longer term, soil chemistry. Air pollution damage reduction Stomata are the main route of entry of gaseous air pollutants into leaves. As stomata1 conductance is reduced at elevated CO, concentrations, it is logical to suppose that CO2 could protect plants from air pollution, or at least reduce the extent of damage [22]. The atmospheric pollutants of concern are sulphur dioxide (SO,), oxidesof nitrogen (NO,), and ozone (0,). In European countries burning of fossil fuel is the main source of gaseous SO2 and motorized vehicles are the main source of NO,. High levels of NO, contribute to increased Oi levels. These gaseous pollutants can cause injury to plants, and reduce their growth. Elevated SO?, 03, and NO, are widely believed to play a major role in the forest dieback observed in central Europe [23]. In some plants. fumigation with SO, or O3 alone caused increased stomata1 opening [24. 251. At high CO1 concentrations. however, stomata1 conductante is reduced and this allows less gaseous pollutants to enter. R. W. Carlson [26] showed that a reduction in
I $ ” ‘\ E > ‘I. “, *’ E “\.\. .Y iE 10 $ $$ f 0I_ 0.0 0.2
, ‘-1.
.450 )III-’ co, \ 0.4
l -. 0.6
SO, Concentration
Water use eficiency The stomata1 response to elevated CO2 concentrations is important in terms of crop productivity, as the efficiency of the plants to use water is greatly increased.
mo cl I-’ co,
0.8
3oo)rllr’
photosynthesis in soya bean, as a response to high SO? levels, was much less in the presence of high levels of CO2 (figure 4). L-Y. Hou et al. [27] showed that high CO.-?concentrations could decrease SO?, Injury to alfalfa and also reduce the Inhibition of photosynthesis caused by SOZ and NO1 mixtures. Ozone leaf injury in the presence of about 800~ I I-’ CO? was reduced by 14 per cent for pinto bean and by 66 per cent for tobacco [28]. Plant-plant interactions Not all plants respond in the same way to elevated CO? concentrations. Doubling of the ambient CO2 levels could have a significant effect on the species distribution. As C3 plants generally benefit more from elevated CO7 concentrations, these will tend to outgrow C4 competitors. For example, in one experiment increasing the atmospheric CO> concentration from 350 to 600 or IO00 ~1 I-~I increased the growth of the C3 weed, velvet leaf (Abutilon theophrust: Medic) relative to the C4 crop, corn [14). A C3 crop would, however, compete more successfully with C4 weeds at elevated CO2 concentrations. Also among C3 plant communities, differences in response to high atmospheric CO? levels lead to one species being a superior competitor. A I : 1 mixture of ryegrass and white clover was sown at ambient and elevated CO? levels (275 and 547~1 1-l CO?). At low CO1 levels ryegrass was clearly the superior competitor, whereas at high CO1 levels clover in the mixture dominated [291. Changes in branching, flowering, fruit and seed production, seed quality, and flower abortion were also observed with elevated levels of atmospheric CO?. Enhanced branching and tillering in high CO? atmospheres has been reported for barley, rice, wheat, soya bean, pea, and rose. Increased branching enables plants to exploit available space better and increases the number of potential flowering and fruiting sites [30]. In a few garden plants. time to flowering and time to maximum floral display was reduced with increasing CO?, [3 I]. The effect of CO7 on flowering IS at least species specific, if not genotype specific. A doubling in flowering by one species without concomitant increase in other insect-pollinated species in that community. could drastically effect pollinator attraction. to the detriment and eventual loss of some species.
co,
1.0
(cl I-‘1
Figure 4 The effect of SO? on photosynthesis of varying COP concentrations for Glycine max. L. after Carlson 1261.
Nutrient availability Plants grown at elevated CO, levels develop more vigorous root systems, which can exploit a larger area of soil for water and plant nutrients. With higher growth yields correspondingly gr;eater amounts of nutrient elements must be 145
E 2
1.3
;
1.2
5 ‘E
1.1
TABLE
2 EFFECT OF HIGH SOIL ATMOSPHERE CO2 CONCENTRATION ON THE MOBILIZATION OF SELECTED CATIONIC SPECIES FROM A GARDEN SOIL
Soil atmosphere
Ca
Solute component,pg K Mg
ml-’ Na
Al
s .h 3 0) a
3% co2 Normal air
1.0 0.9 440
540
640
CO2 Concentration
740
840
CO2 and the soil environment
The CO* concentration in the soil atmosphere tends to be 10 to 100 times greater than that in the above-ground atmosphere because of continued generation of COz by biological processes (mainly
1987
ONDJF
M
A
1988
Figure 6 Seasonal variations in soil atmospheric COP concentrations at 300 mm depth for an upland moor in north-east Scotland.
146
0.47 0.34
0.35 0.27
0.11 0.09
940
absorbed through the roots. R. J. Luxmoore et al. [32] showed that one-yearold pine seedlings took up more N and other plant nutrients from the soil at elevated CO2 concentrations (figure 5). Their results also showed that, at particularly high levels of COz, P and K were used more efficiently and less P, K, and NO3 were leached from soil. For plants grown at elevated CO2 concentrations for long periods, however, one can envisage an eventual decrease in nutrients available in the soil. Nutrient deficiencies cause stress in plants, decrease the yield, and possibly change the frost hardiness, which could also make them more vulnerable to insect attacks and viral infections. It cannot, therefore, be ruled out that rising atmospheric CO2 concentrations have contributed to forest dieback observed in Central Europe. If CO2 is a contributing factor, diverse symptoms might be anticipated at different sites. Although the rising CO* concentrations in this casewould be beneficial in protecting the forests from SO2 and 0s injuries, faster growth could lead to nutrient deficiencies and soil acidification on susceptible soils. The latter could, in turn, lead to freshwater acidification.
S
0.41 0.27
(pl I-‘)
Figure 5 Effect of atmospheric CO2 concentration on Ca, N, Mg, and P in Virginia Pine seedlings, extracted from data of Luxmooreet a/. 1321. Contents are relative to amounts at 340~1 I-’ CO*.
A
0.15 0.11
M
root and microbial respiration). In upland moorland soils in the north-east of Scotland, soil atmospheric CO?, levels between 1 and 2 per cent (10000-20000 ~1 1-l CO*) are not unusual (Skiba and Cresser, unpublished results, figure 6). Soil CO2 concentrations vary with temperature and moisture content of the soil. Highest concentrations are usually recorded in the summer months. Elevated atmospheric CO2 concentrations increase plant growth, which also results in development of more vigorous roots. Microbial populations are stimulated in the vicinity of plant roots (the rhizosphere) as a result of the release of organic substances from the roots and the decay of old root cells. With more vigorous root systems, the surface area of the rhizosphere increases and more root-derived substances are released. Bigger plants will also produce more litter and other plant debris. Overall it can be expected that the amounts of organic substances added to the soil will be increased. Indirectly, elevated atmospheric CO2 concentrations, therefore, should enhance biological activity in the soil. Under aerobic conditions this means an increased consumption of 02 with subsequent release of COz. A large proportion of the soil CO* will diffuse to the surface and then into the atmosphere. It can be expected that an even further substantial increase in atmospheric CO* may result from increased soil respiration. As postulated above, faster growth may deplete nutrients in the soil. On the other hand, stimulated microbial activity in the soil may turn over the organic matter at a quicker rate; that is, may release more nutrients for plant growth. Most plant nutrients, however, are available for both plants and microorganisms, so that significant amounts may be temporarily immobilized as microbial biomass. Increasing the input of organic matter into soil may accelerate the acidification of the soil, especially if base cation supply is limited and litter accumulation increases. Enhanced uptake of cations by faster growing plants will have the same effect. The present authors have shown that when a garden soil was equilibrated with a high concentration of CO* (3 per cent) by flushing with an appropriate gas mixture, and subsequently leached with rainwater, more
cations were leached from the soils treated with 3 per cent CO2 than with air (Table 2, Skiba and Cresser, unpublished results). This process also could accelerate the development of nutrient deficiencies and soil acidification. It appears, therefore, that elevated atmospheric CO* concentrations could well have adverse effects on the soil environment in the long term. On managed land, soil acidification and nutrient deficiences can be alleviated by fertilization. Large forested areas and upland moorland sites could be expected to suffer, however. Much more research is needed to show conclusively long-term effects of elevated atmospheric CO* concentrations on soil/plant interactions.
Conclusion
Much of what has been said so far is factual, but some is, of necessity, speculative. We have not considered possible implications of plant physiological changes which might be induced by increased CO2 in terms of food quality for higher organisms, from insects through to man. This is deliberate, because so little is known. Thus, if a single conclusion is to be reached, it must be that there is a vital and urgent need for research on potential ecological effects on a broad front. Climatic change modellers have led the way, but they could be studying the tip of a potentially very damaging iceberg.
Acknowledgements
The authors are indebted to the DOE (UK) and NERC for financial support and to Sarah Woodin for figure 2.
References
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147