Biological Consequences of Increased Concentrations of Atmospheric CO2

Sherwood B. Idso

For most of the past two millennia, the carbon-dioxide content of earth's atmosphere has been amazingly constant, hovering at a mean concentration of approximately 280 parts per million (ppm). With the dawning of the Industrial Revolution, however, this equilibrium was disturbed: the CO2 content of the air began to rise as humanity embarked upon a course of unprecedented economic development that was fueled by the burning of massive quantities of coal, gas, and oil, which released huge amounts of carbon dioxide into the atmosphere.

The rise in the concentration of atmospheric CO2 that has accompanied this societal transformation is currently viewed with considerable alarm, due to its purported ability to induce what many believe will be catastrophic global warming. But the phenomenon is not without its positive aspects, among which is its ability to stimulate vegetative productivity and it is possible that this demonstrable biological consequence of increased concentrations of atmospheric CO2 may ultimately prove to be of far greater significance than its speculative climatic consequences. Hence, it is important to review what we know about the little-publicized effects of increased concentrations of atmospheric CO2 on the growth and development of plants; for these are the only effects of the rising CO2 content of earth's atmosphere about which we can be truly confident.

Effects of CO2 upon plant growth

Carbon dioxide is the basis of almost all life on earth as it is the primary raw material used by plants to produce organic matter. Rogers et al. (1992) have highlighted this fact by noting that carbon dioxide is the first molecular link between the atmosphere and biosphere, that it is essential for photosynthesis, which sustains plant life, the basis of the entire food chain, and that no substance is more pivotal for ecosystems, either natural or managed. The veracity of these claims is supported by literally hundreds of experiments that have convincingly demonstrated that the more CO2 there is in the air, the better plants perform their many vital functions. In the first major review of this subject (Kimball 1983a), which was based upon 430 individual experimental results, Kimball observed that the productivity of most herbaceous plants rose by about one-third in response to a doubling of the air's CO2 content (330 to 660 ppm); and in a subsequent analysis of 770 sets of measurements, he obtained essentially the same result (Kimball 1983b). Other reviews have revealed similar or even larger CO2-induced growth enhancements (Lemon 1983; Cure and Acock 1986; Mortensen 1987; Lawlor and Mitchell 1991; Drake 1992a; Poorter 1993; Ceulemans and Mousseau 1994; Strain and Cure 1994; Wullschleger et al. 1995, 1997); while in the most comprehensive study of all, which reviewed the results of over 1000 laboratory and field experiments conducted subsequent to the time of Kimball's analyses, Idso (1992a) documented a mean productivity enhancement of 52 percent in response to a 300 ppm increase in the air's CO2 content.

This positive response of plants to increases in the concentration of atmospheric CO2 cuts across all botanical boundaries and is present, to a greater or lesser degree, in all types of vegetation (Poorter 1993). Indeed, it is now realized to be one of the verities of nature that, with more CO2 in the air, plants generally grow larger, have more branches or tillers, more and thicker leaves, more extensive root systems, as well as more flowers and fruit (Idso 1989a); and in consequence of these well established facts, Sylvan H. Wittwer, the father of modern research in this area, stated recently that "it should be considered good fortune that we are living in a world of gradually increasing levels of atmospheric CO2" (1997: 13). As we shall shortly see, we have already reaped immense benefits from this phenomenon and we can anticipate even greater positive consequences in the years ahead.

Effects of CO2 upon the efficient use of water by plants

In addition to enhancing vegetative productivity, an increase in the concentration of atmospheric CO2 tends to reduce the apertures of the small pores or stomates through which water vapor escapes from plant leaves and is lost to the atmosphere (Pallas 1965; Morison 1985). The reduction in rate of evaporation from leaves produced by this phenomenon averages about one-third for a doubling of the air's CO2 content (Kimball and Idso 1983; Cure and Acock 1986); and combining this effect with the simultaneous CO2-induced increase in plant productivity actually doubles the efficiency with which individual leaves utilize water to produce organic matter.

The likely consequences of this phenomenon are truly impressive. As the concentration of atmospheric carbon dioxide rises ever higher in the years ahead, plants should be able to grow where it is presently too dry for them, enabling the most drought-resistant species to reclaim great tracts of land previously lost to desertification (Idso and Quinn 1983; Idso 1989b). Greater vegetative cover should also reduce the adverse effects of soil erosion caused by the ravages of wind and rain (Idso 1991a). And, with greater plant productivity both above-ground (as noted in the previous section) and below-ground (Idso et al. 1988; Rogers et al. 1994; Jongen et al. 1995; Pregitzer et al. 1995; Tingey et al. 1996), there is typically an increase in soil organic matter (Lekkerkerk et al. 1990; Wood et al. 1994; Sombroek 1995; Henning et al. 1996; Batjes and Sombroek 1997; King et al. 1997; Prior et al. 1997), which usually produces even further benefits.

Creatures such as earthworms that live in the soil are greatly stimulated by additions of organic matter (Edwards 1988; Rogers et al. 1994); and an increase in their activity would likely lead to the creation of much new soil (Graham et al. 1988; Johnson 1988) while at the same time improving the fertility, structure, aeration, and drainage of existing soils (Edwards 1997). These improvements, in turn, would likely boost plant productivity even higher, putting still more organic matter into the soil, and so on (Idso 1991b), as the several phenomena reinforce each other to lift the whole biosphere to a new level of activity (Idso 1992b).

The challenge of inadequate resources

In spite of the impressive body of evidence that has established the reality of the many biological benefits of an atmosphere enriched with increased concentrations of CO2, many find it difficult to believe that a gaseous effluent of our industrial society might be good for the biosphere (Gore 1992); and, from time to time, a few scientists have suggested that the limited availability of resources characteristic of unmanaged ecosystems will reduce or even totally negate the growth-enhancing effects of increased concentrations of atmospheric CO2 upon natural (as opposed to managed, i.e. agricultural) plant communities (Kramer 1981; Oechel and Strain 1985; Bazzaz and Fajer 1992). Consequently, in an effort to resolve this issue, Idso and Idso (1994) reviewed the plant science literature of the 10-year period following the original reviews of Kimball (1983a, b) and analyzed the results of all paired sets of CO2-enrichment experiments that were conducted simultaneously under growing conditions that were both ideal and less than ideal. Results of their several findings are summarized in the following subsections.

Low levels of light

Decreasing light intensity had no significant effect upon plants' photosynthetic response to increased concentrations of atmospheric CO2 until the lowest light intensity of the 37 experiments studied was encountered. At that level, contrary to the contentions of those who view inadequate resources as impediments to the positive effects of increased concentrations of CO2, there was a rise in CO2-induced benefits: the mean percentage increase in photosynthesis due to a 300 ppm increase in atmospheric CO2 rose from 68 percent under normal light intensities to 80 percent at the lowest light intensity studied, while the mean percentage increase in photosynthesis due to a 600 ppm increase in CO2 rose from 111 percent to 194 percent.

Studies published subsequent to the review of Idso and Idso (1994) have continued to demonstrate that low light intensities do not negate the beneficial effects of increased concentrations of atmospheric CO2 upon plant growth and development (Maruyama and Huang 1996; Percival et al. 1996; Wang 1996; Kubiske and Pregitzer 1997). In fact, in a study of plants in the forest understory, Osborne et al. (1997) found that elevated CO2 concentrations allowed for a positive net photosynthetic uptake of carbon on days and at locations that typically experienced light intensities so low that they were generally insufficient for positive net photosynthesis under current atmospheric CO2 concentrations, i.e., they found that elevated CO2 concentrations allowed the plants to live where they currently cannot due to a lack of sufficient light. Hence, they concluded that "the potential range of habitats that such species could occupy will expand considerably with rising atmospheric CO2" (1997: 343); similar conclusions are suggested by the work of Caporn et al. (1994); Wang et al. (1995); Kubiske and Pregitzer (1996), and Liang et al. (1996).

Inadequate water

When lack of water posed a limitation to vegetative growth and development, the results of Idso and Idso's (1994) analyses of 55 experiments were even more dramatic than those pertaining to low light levels. The growth enhancement caused by a 300 ppm increase in atmospheric CO2 jumped from 31 percent when water supplies were optimal to 63 percent when they were less than optimal while, for an increase of 600 ppm in the concentration of CO2, the CO2-induced growth enhancement jumped from 51 percent to 219 percent when the availability of water decreased from adequate to less than adequate. Here, too, subsequent studies continue to support these general observations (Liang and Maruyama 1995; Roden and Ball 1996; Goodfellow et al. 1997) and, in a model-driven review of experimentally established principles derived from work on temperate forest species, Thornley and Cannell have independently concluded that the on-going rise in the air's CO2 content "will protect trees from debilitating water stress" (1996: 1343). Kellomaki and Wang (1996) have come to the same conclusion as a result of their own observations and, in much the same vein, Polley et al. (1996) have observed that a doubling of the concentration of atmospheric CO2 can significantly enhance the percentage of seedlings surviving when water is withheld.

Insufficient soil nutrients

In Idso and Idso's (1994) analysis of the effects of limitations of soil nutrients, the growth enhancement due to a 300 ppm rise in the air's CO2 content exhibited a slight decline, dropping from 51 percent to 45 percent when, in a group of 70 experiments, nutrients went from a level that did not limit growth to a level that did. But when the concentration of atmospheric CO2 increased to 600 ppm, this slight negative trend reversed itself, going from a 43 percent CO2-induced growth stimulation when nutrients were present in abundance to a 52 percent enhancement when their supply was sub-optimal. And, with a 1200 ppm increase in atmospheric CO2, growth enhancement jumped from 60 percent when the soil nutrient supply was adequate to 207 percent when it was less than adequate.

Examples from specific ecosystems

Detailed investigations of several managed and unmanaged ecosystems have provided striking examples of how increased concentrations of atmospheric CO2 can endow plants with the capacities they need to overcome the restrictions upon growth that result from limited resources (Koch and Mooney 1996a). In years when the productivities of these plant communities have been unusually high, for example, the effects of elevated concentrations of CO2 have been decidedly moderate; but when environmental factors have combined to curtail their growth and development severely, the effects of increased concentrations of atmospheric CO2 have typically been much more dramatic (Koch and Mooney 1996b).

In the case of a Kansas tallgrass prairie, doubling the atmospheric CO2 concentration enhanced vegetative productivity by only 5 to 10 percent in several years of high productivity but, in a year of intermediate productivity, it increased growth by approximately 40 percent and, in a year of very low productivity, it boosted production by nearly 80 percent (Owensby et al. 1996). Another place where this phenomenon has been observed is in the world's most comprehensive set of Free-Air CO2 Enrichment (FACE) experiments (Hendrey et al. 1993; Dugas and Pinter 1994). In a study where CO2 was injected directly into the air over a wheat crop growing in a field devoid of any alterations to the natural environment, the imposition of a yield-reducing water stress raised the productivity enhancement created by a 180 ppm increase in atmospheric CO2 from 10 percent to 23 percent in two different years (Pinter et al. 1996). Further, in a cotton crop where the wetter of two irrigation regimes reduced the yield resulting from the ambient-air treatment, it was the over-watered plants with lower yield that experienced the greater CO2-induced stimulation to growth in two different years (Pinter et al. 1996).

How high CO2 levels help plants overcome resource deficiencies

One reason that plants are able to respond positively to increased levels of atmospheric CO2 when limited resources significantly curtail their growth is that plants grown at elevated concentrations of CO2 typically have more extensive and active root systems than control plants growing in normal air (Curtis et al. 1990, 1994; Idso and Kimball 1991a, 1992b; Norby 1994; Prior et al. 1995; Gebauer et al. 1996; King et al. 1996; Kubiske et al. 1997), which allows them to explore more thoroughly larger volumes of soil in search of the things they need (Norby et al. 1992; Rogers et al. 1992; Stulen and den Hertog 1993). When more nutrients are encountered in the course of this activity, plants can also acquire them more effectively (Luxmoore et al. 1986; Norby et al. 1986) because the uptake of many essential elements requires the expenditure of metabolic energy (Pitman 1977; Jackson et al. 1980), and the enhanced availability of carbohydrates typically provided by the enrichment of the air with CO2 tends to promote this process (Clement et al. 1978; Rufty et al. 1989; Rogers et al. 1994). A low level of nitrogen in the soil, in particular, is not an impediment to CO2-induced growth enhancement because plants exposed to elevated concentrations of atmospheric CO2 do not need to invest as much nitrogen in their photosynthetic apparatus (Stitt 1991) as it operates so much more efficiently at higher CO2 levels (Nie et al. 1995). Hence, even in the face of severe nutrient deficiencies, plants' photosynthetic rates may be significantly stimulated by increased concentrations of atmospheric CO2 (Norby et al. 1992; Wullschleger et al. 1992), setting in motion still other beneficial phenomena.

One of the most important of these secondary or indirect consequences of CO2-induced growth stimulation in situations where resources are limited is the enhancement of the activity of soil microorganisms (Lamborg et al. 1983; Pregitzer et al. 1995; Tingey et al. 1996) that is provided by enhanced root exudation of organic substances (Norby 1997; Hungate et al. 1997). This enhanced activity of microorganisms typically stimulates a multiplicity of growth-promoting effects beneath the soil surface (Zak et al. 1993). As the "better-fed" hyphae (filamentous structures) (Smith and Read 1996) of more numerous and robust symbiotic fungi extend outward from their CO2-enriched hosts (Ineichen et al. 1995), for example, they lengthen the life of absorptive root hairs (Fogel 1983) and increase the area of root surface available for water and nutrient uptake (Tinker 1984; Clarkson 1985; Smith and Read 1996). The microscopic organisms that live in the plant's root zone or rhizosphere also secrete a number of organic acids that hasten the chemical weathering of soil minerals (Boyle and Voigt 1973; Boyle et al. 1974) and they are especially adept at making phosphorus available to plants by this means (Ortuno et al. 1978; Molla et al. 1984; Babenko et al. 1985). In addition, these microscopic organisms produce a variety of hormones that stimulate root growth (Simmons and Pope 1987, 1988), enhancing the production of lateral roots and root hairs (Umali-Garcia et al. 1980; Kapulnik et al. 1983).

Most important of all, perhaps, is the ability of elevated levels of atmospheric CO2 to stimulate the activity of nitrogen-fixing bacteria directly (Burk 1961; Lowe and Evans 1962). The capacity of these bacteria to remove nitrogen from the atmosphere and make it available to plants appears to be limited by their host plants' rates of carbohydrate production (Sinclair and de Wit 1975; Hardy et al. 1976; Finn and Brun 1982). Consequently, anything that stimulates vegetative productivity, including increased concentrations of atmospheric CO2, generally stimulates bacterial nodule growth and activity (Quebedeaux et al. 1975; Murphy 1986) and several-fold increases in the air's CO2 content have indeed been found to produce several-fold increases in nitrogen fixation in a number of experiments (Hardy and Havelka 1973, 1975; Havelka and Hardy 1976; Phillips et al. 1976; Hardy et al. 1978; MacDowall 1983).

Acting in concert, these phenomena typically allow the growth-enhancing effects of increased concentrations of atmospheric CO2 to be expressed in the face of severe nutritional deficiencies, suggesting that carbon starvation (Svedang 1992; Cizkova-Koncalova et al. 1992; Robinson 1994) may well be a more significant impediment to the growth of the planet's vegetation than is a lack of soil nutrients. In the words of Gunderson and Wullschleger, who have reviewed the subject in depth, "hypotheses that either nutrient or water limitations would limit photosynthetic responses in natural environments have not been adequately supported by the currently available data" (1994: 384). Quite to the contrary, the data demonstrate, as noted by Gifford, that "high CO2 increases light-use efficiency, water-use efficiency and nitrogen-use efficiency," so that "the Ôlaw of limiting factor' concept that such vegetation cannot respond to increased CO2 concentration does not apply to C3 species  [C3 plant species are distinguished from C4 plant species in that they use the process of photosynthesis first identified by science, a process using an enzyme that reacts with both CO2 and O2 and that is, thus, less efficient in the presence of relatively higher levels of O2 than the process used by C4 plant species, which depends upon a different enzyme that does not interact with O2. Increased concentrations of atmospheric CO2 are, therefore, of much greater benefit to C3 species of plants than to C4 species. The names come from the three-carbon (C3) sugar that is the first product of the photosynthetic process in C3 species and from the four-carbon (C4) organic acid that is the first product in C4 species.]" (1994: 33) which include fully 95 percent of all of earth's plants (Drake 1992b; Bowes 1993).

The challenge of environmental stresses

In addition to limited resources, there are a number of environmental stresses that are typically encountered in natural and agricultural ecosystems and it has been claimed that their debilitating influences reduce or negate the benefits that can accrue to plants from increased concentrations of atmospheric CO2. The review of Idso and Idso (1994) demonstrates once again, however, that such effects are generally not observed in laboratory and field experiments and that, if anything, just the opposite is more likely to occur.

Soil salinity and air pollution

In an analysis of 42 sets of measurements of the reponse of plant growth to increased concentrations of atmospheric CO2 at different values of soil salinity, Idso and Idso (1994) found that the growth-promoting effects of elevated levels of CO2 in the air were found to about the same degree in plants stessed by increased salinity of the soil as in plants in soil of normal salinity, demonstrating that, on average, soil salinity does not reduce the biological benefits of increased concentrations of atmospheric CO2. What is more, in another 20 sets of measurements, when air pollutants were the source of stress, the percentage enhancement in growth brought about by a 300 ppm increase in atmospheric CO2 actually rose in the face of this adversity, from 38 percent when air pollutants were absent to 54 percent when they were present in noxious quantities. And, as was the case where there were limited resources, research conducted subsequent to the review of Idso and Idso (1994) has continued to confirm their basic finding about the interaction between CO2 and air pollution: a doubling of the air's CO2 content was often found to compensate totally for the debilitating effects of air pollutants such as ozone (Rudorff et al. 1996; Volin and Reich 1996; McKee et al. 1997; Mulholland et al. 1997; Fiscus et al. 1997).

Global warming

The environmental stress about which certain scientists-and, therefore, the Press and the public-seem to worry most is that produced by higher air temperatures (Peters and Darling 1985; Paine 1988; Davis 1989; Woodwell 1989; Gear and Huntley 1991; Dobson 1992). They are concerned that future global warming may be so great that plants will need to migrate towards the poles in order to remain within the climatic regimes to which they are currently best suited (Overpeck et al. 1991; Dyer 1995) and, because the warming is predicted to be so rapid, they fear that many plants may not be able to migrate fast enough to avoid extinction (Possingham 1993; Root and Schneider 1993; Pitelka et al. 1997).

Although this scenario may sound reasonable, it is largely contradicted by basic research into plant physiology. In an analysis of 42 different data sets, Idso and Idso (1994), for example, found that the growth enhancement due to a 300 ppm increase in atmospheric CO2 actually rose with increasing air temperature, climbing from nearly 0 percent at 10șC to a full 100 percent at 38șC; for greater increases in the air's CO2 content, the percentage of growth enhancement was greater still, something that ongoing research continues to confirm (Nijs and Impens 1996; Vu et al. 1997).

One reason for this counter-intuitive response is that the optimum temperature for plant growth generally rises as the air's CO2 content rises (Berry and Bjorkman 1980; Taiz and Zeiger 1991; McMurtrie et al. 1992; McMurtrie and Wang 1993). Long (1991), for example, has calculated from basic principles of plant physiology that a 300 ppm increase in atmospheric CO2 should cause the optimum temperatures of most C3 plants to rise by about 5șC; an analysis of the results of 7 studies that have experimentally evaluated this phenomenon (Bjorkman et al. 1978; Nilsen et al. 1983; Jurik et al. 1984; Seemann et al. 1984; Harley et al. 1986; Stuhlfauth and Fock 1990; McMurtrie et al. 1992) reveals a mean optimum temperature rise of 5.9șC with a 300 ppm increase in atmospheric CO2 (Idso and Idso 1994). And, as this rise in optimum temperature is even larger than the rise in air temperature predicted to result from the greenhouse warming caused by such a CO2 increase (IPCC 1990, IPCC I 1996), a CO2-induced warming would not adversely affect the vast majority of earth's plants, 95 percent of which are of the C3 variety (Drake 1992b; Bowes 1993). In addition, the remainder of the planet's species-which may not experience quite as large a rise in optimum temperature (Chen et al. 1994)-are already adapted to earth's warmer environments (De Jong et al. 1982; Drake 1989; Johnson et al. 1993), which are expected to warm much less than the other portions of the globe (IPCC 1990, IPCC I 1996).

In view of these facts, it is clear that a CO2-induced global warming would not produce massive poleward migrations of plants seeking cooler weather, for the temperatures at which nearly all plants perform at their optimum would rise at the same rate as (or faster than) and to the same degree as (or higher than) the temperatures of their respective environments. What is more, the photosynthetic rates of the 7 plants for which these evaluations have been experimentally derived were found to be nearly twice as great at their CO2-enriched optimum temperatures as they were at their optimum temperatures under present CO2 conditions (Idso and Idso 1994), suggesting not only that typically predicted increases in atmospheric CO2 and global air temperatures would not hurt earth's vegetation, but also that they might actually help it, as subsequent investigations have revealed as well (Wang 1996).

Finally, at the highest air temperatures encountered by plants, increased concentrations of atmospheric CO2 have been demonstrated to be especially valuable for they often mean the difference between life and death (Rowland-Bamford et al. 1996; Idso 1997), as they typically enable plants to maintain positive carbon exchange rates in situations where plants growing under present CO2 concentrations exhibit negative rates that ultimately lead to their demise (Idso et al. 1989, 1995). Faria et al. (1996) have studied this phenomenon in detail in seedling oak trees and believe that the life-sustaining function of increased concentrations of atmospheric CO2 at high air temperatures may also be partly due to a stabilization of enzymes susceptible to heat through the increased concentration of sugars generally found in CO2-enriched leaves.

Long-term exposure to increased concentrations of CO2

Most studies of plants' responses to increased concentrations of atmospheric CO2 have been of rather short duration, ranging from hours to days to weeks. Some agricultural investigations have lasted longer, encompassing entire growing seasons; even in the case of long-lived plants, such as trees, however, few experiments have had their durations measured in years. Consequently, there has always been a concern that results derived from short-term experiments may not apply to plants over the longer term; and, in fact, there is an experimental basis for this worry.

Acclimation to high CO2

According to a concept variously referred to as "acclimation" or "down regulation," it is believed by some biologists that long-term exposure to elevated levels of carbon dioxide will result in a reduction of the photosynthetic capacity of plants. This contention is based on the results of a number of experiments that have indeed revealed such behaviour in several plants (Kramer 1981; Pearcy and Bjorkman 1983; Delucia et al. 1985; Cure and Acock 1986; Tissue and Oechel 1987) and, although it is possible that such a phenomenon may regularly occur in certain species (Sicher and Bunce 1997), and that it may occur more generally under certain circumstances (Lewis et al. 1994; Luo et al. 1994; Reining 1994; Ziska et al. 1995; Marek and Kalina 1996; Micallef et al. 1996), there are reasons to believe that it is not expressed-or not as consistently expressed (Sicher and Kremer 1994; Van Oosten and Besford 1996)-in the majority of plants growing in natural situations.

Many of the experiments that have exhibited long-term declines in CO2-induced benefits to plants, for example, have been conducted in controlled environments or greenhouses (Drake and Leadley 1991), where the plants that were studied were grown in pots or some other type of root-restricting container. As a number of studies have demonstrated (Masle et al. 1990; Arp 1991; Hogan et al. 1991; Thomas and Strain 1991; Samuelson and Seiler 1992), root restrictions may sometimes prevent the full expression of the effects of increased concentrations of atmospheric CO2, particularly when the plants grow larger, a natural consequence of longer experiments.

In contrast to the results of studies in controlled environments, long-term field experiments often show no reductions in the photosynthetic capacities of plants exposed to elevated concentrations of CO2 (Radin et al. 1987; Sage et al. 1989; Idso and Kimball 1991b; Norby and O'Neill 1991; Gunderson et al. 1993; Dufrene et al. 1993; Jones et al. 1995; Teskey 1995, 1997; Wang and Kellomaki 1997), or they show an actual increase or "up regulation" in photosynthesis and growth over extended periods of time (Campbell et al. 1988; Conroy 1989; Chen and Sung 1990; Ziska et al. 1990; Arp and Drake 1991; Long and Drake 1991; Drake 1992c; Barton et al. 1993; Vogel and Curtis 1995; Liu and Teskey 1995; Jacob et al. 1995). There has been one field experiment that produced a contrary result (Oechel and Strain 1985; Tissue and Oechel 1987; Grulke et al. 1990) but the Arctic tussock tundra of that study was growing close to the temperature (10șC) at which its response to increased concentrations of atmospheric CO2 truly should have been near zero, according to the analysis of temperature effects in the review of Idso and Idso (1994) and in harmony with the published opinions of several scientists who have analyzed this particular experiment in some detail (Drake and Leadley 1991; Long 1991; Drake 1992c; Kirschbaum 1994; Webber et al. 1994). What is more, in a subsequent three-year study of this same ecosystem, an artificially imposed warming of only 4șC totally eliminated the down regulation observed at current air temperatures (Field 1994; Oechel et al. 1994). Consequently, although not to be ruled out in all instances, down regulation of photosynthesis and growth does not appear to be a major impediment to the long-term effectiveness of the aerial fertilization effect of increased concentrations of atmospheric CO2 in stimulating the productivity of earth's vegetation for, as Woodrow has concluded after reviewing the subject in considerable depth, "C3 plants probably possess the genetic feedback mechanisms required to efficiently Ôsmooth out' any imbalance within the photosynthetic system caused by a rise in atmospheric CO2" (1994: 401) so that, in the words of Amthor, "acclimation . . . of photosynthesis to increasing CO2 concentration is unlikely to be complete" (1995: 243).

The world's longest experiment studying
increased concentration of CO2

In the longest study of its kind ever to be conducted-and where down-regulation would be expected to appear if it were a truly ubiquitous consequence of long-term exposure to increased concentrations of CO2-my colleagues and I planted 8 seedling sour-orange trees directly into the ground at Phoenix, Arizona, in July of 1987 and enclosed them in pairs within 4 open-topped chambers made of clear polyethylene film. Then, in November of that year, we began to pump air with a CO2 concentration of 700 ppm continuously into two of the enclosures through perforated plastic tubes that lay upon the ground while we pumped ambient air with a CO2 concentration of 400 ppm into the other two enclosures (Idso et al. 1991). This protocol we have faithfully maintained to the present day, documenting the course of the effects of increased concentrations of atmospheric CO2 upon the trees as they have progressed from tiny seedlings through the juvenile stage of development and into full maturity, which they appear to have reached about two years ago.

The results of this decade-long experiment have been truly remarkable. Over the entire course of the study, the CO2-enriched trees, which receive 75 percent more CO2 than the control trees-have continually produced over twice as much biomass as the trees growing in normal air (Idso and Kimball 1997); at our last harvest, we picked over three times as much fruit from the trees exposed to the extra CO2. Hence, although we intend to continue the experiment for several more years and do not yet have the final word on the subject, we feel confident that the beneficial effects of increased concentrations of atmospheric CO2 observed to date will likely persist over the entire life span of the trees.

Historical trends in forest productivity

In addition to the experiments of scientists, the biosphere itself is providing evidence for the reality and long-term sustainability of the aerial-fertilization effects of increased concentrations of atmospheric CO2. In the southwestern United States, for example, there is considerable evidence that the woody plants that were present in pre-industrial times, when the air's CO2 content was much lower than now, were somewhat stunted compared to their present-day descendants (Johnston 1963; Scifres 1980). This phenomenon was not fully appreciated, however, until LaMarche et al. published a paper (1984) describing an analysis of annual growth rings obtained from pine trees growing near the timberline in California, Colorado, Nevada, and New Mexico. All of the trees that they studied exhibited large increases in growth rate between 1859 and 1983 and some of them doubled their productivity during this time. The researchers noted that the increased growth rates exceeded those expected from climatic trends but were consistent in magnitude with what would be expected from the historical trend of increasing concentrations of atmospheric CO2, a trend particularly pronounced in recent decades.

Reports of a similar nature followed in quick succession. Along the western coast of North America, conifers growing in the high altitudes of the Cascade Mountains of Washington were found to have increased their growth rates by approximately 60 percent since 1890 (Graumlich et al. 1989). In British Columbia, ring-width measurements of Douglas firs also revealed a marked increase in growth in recent decades and Parker noted that "environmental influences other than increased CO2 have not been found that would explain [the phenomenon]" (1987: 511).

In New England, a study of a 320-year-old Pinus rigida rock-outcrop community showed its trees to have experienced a dramatic increase in growth since 1970 (Abrams and Orwig 1995). Another study of 10 tree species revealed a mean growth enhancement of 24 percent from 1950 to 1980 (Hornbeck et al. 1988). In Georgia, annual growth increments of long-leaf pines began to rise dramatically about 1920, increasing by approximately 30 percent by the mid-1980s (West 1988). In this study, too, it was reported that the increased growth could not be explained by trends in either precipitation or temperature, leaving the rising CO2 content of the air as the most likely cause of the increase in productivity.

In between these regions, the growth rates of several hardwoods in the Great Smokey Mountains also increased over the last half-century (Busing 1989), as did those of other conifers in other regions of both the United States (Jacoby 1986; Graybill 1987; Hornbeck 1987; Kienast and Luxmoore 1988) and Canada (Jozsa and Powell 1987). In one such study, a colleague and I analyzed data collected from long-lived bristlecone, foxtail, and limber pines at high-altitude sites in Arizona, California, Colorado, and Nevada (Graybill and Idso 1993). In almost all of the chronologies we developed, a sharp upward growth trend began about the middle of the 1850s and has continued to the present. No comparable variations were observed anywhere else in the records, which continued back in time almost two millennia, suggesting that the accelerating growth observed in the last century-and-a-half of the several chronologies were truly unique and the result of some major regional or global factor. Furthermore, comparisons of the chronologies with records of changes in temperature and precipitation ruled out the possibility that either of these climatic variables played a significant role in enhancing the trees' growth rates, strongly implicating the rise in the air's CO2 content as the factor responsible for the trees' increasing productivities over the past 150 years.

In Europe, a number of field studies have told much the same story. In forests of silver firs in the mountains of northeastern France, radial growth measurements have revealed a productivity increase of nearly 70 percent from 1830 to 1935 (Becker 1989) and the last decades of the century have seen significant increases in the growth of beech and spruce stands in southern Sweden (Bjorkdahl and Eriksson 1989; Falkengren-Grerup and Eriksson 1990). Similarly, stands of Scots pine in northern Finland have experienced growth increases ranging from 15 to 43 percent between 1950 and 1983 (Hari et al. 1984; Hari and Arovaara 1988). Since CO2 is the only environmental factor that has changed systematically during this century in the remote area of this study, it was thus to this factor that Hari and Aravaara attributed the increased growth of the trees.

Germany presents an even more intriguing situation. In the late 1970s and early 1980s, reports of a large-scale decline in forest productivity were commonplace. When detailed studies based on extensive measurements finally appeared, however, just the opposite proved to be true (Eichkorn 1986; Glatzel et al. 1987; Spelsberg 1987). From the middle of the 1950s at the latest, Norway spruce, silver fir, and beech have all showed remarkable increases in growth rate (Kenk 1989; Spieker 1990), not following the normal age trend (Kenk and Fischer 1988); the growth of pine likewise increased (Pretzsch 1985a, 1985b). By the end of the 1980s, yields of most European forests were clearly above normal (Innes and Cook 1989). In early 1992, for example, scientists from the Finnish Forest Research Institute reported a general increase in forest growth in Austria, Finland, France, Germany, Sweden, and Switzerland (Kauppi et al. 1992) and Weidenbach (1992) reported that annual growth increments in the German state of Baden-WŸrttemberg had risen approximately 20 percent in just the past 20 years.

Possibly the most revealing observations of all are those that come from tropical forests. Noting that the turnover rates of mature tropical woodlands correlate well with measures of their net productivity (Weaver and Murphy 1990), Phillips and Gentry (1994) assessed the turnover rates of forty tropical forests from around the world in order to test the hypothesis that forest productivity is increasing globally. Not surprisingly in view of the material just reviewed, they found that the turnover rates of these highly productive tropical woodlands have indeed been rising ever higher since 1960, if not earlier, and that there seems to have been a worldwide acceleration of this trend since about 1980. They also noted that "the accelerating increase in turnover coincides with an accelerating buildup of CO2" (Phillips and Gentry 1994: 957). And as Pimm and Sugden stated in a companion article, it was "the consistency and simultaneity of the changes on several continents that [led] Phillips and Gentry to their conclusion that enhanced productivity induced by increased CO2 is the most plausible candidate for the cause of the increased turnover" (1994: 933-34).

The breath of the biosphere

Compelling evidence for increasing stimulation of earth's plant life by the ongoing rise in the atmosphere's CO2 concentration is to be found in the air itself. Each spring, when the northern hemisphere's thin veneer of vegetation awakens from the dormancy of winter and begins a new season of growth, it draws enough carbon dioxide out of the air to reduce the concentraton of atmospheric CO2 by several parts per million. In the fall, when much of this vegetation dies, it releases huge quantities of carbon dioxide back to the air, causing the CO2 content of the atmosphere to rise by a small amount. Meticulous measurements obtained over the past four decades have clearly demonstrated that the difference between the high and low points of this seasonal oscillation-this "breath of the biosphere" (Idso 1995)-is growing ever larger. Several groups of scientists have studied the phenomenon in detail and nearly all of them have concluded that it implies that the photosynthetic activity of the earth's plant life is growing greater and greater each year; many suggest that the ever-increasing aerial fertilization effect of the steadily rising CO2 content of the atmosphere is its primary cause.

Working with data for atmospheric CO2 from Mauna Loa Observatory in Hawaii, Point Barrow in Alaska, and Weather Station P in the North Pacific Ocean, Pearman and Hyson (1981) concluded that "it is most probable that there has been an increase in the summer net ecosystem production of the Northern Hemisphere of 8.6 percent over the period 1958-1978," stating that "the results are consistent with the concept of enhanced activity due to increased levels of CO2" (1981: 9842). Two years later, Cleveland et al. (1983) confirmed this finding with additional data from Mauna Loa and a companion record from the South Pole, stating: "we believe it most likely that the CO2 seasonal behaviour reflects an increase in either the seasonally varying biomass or in global photosynthetic activity resulting from the increasing concentration of atmospheric carbon dioxide" (1983: 10,945). Two years later, Keeling et al. (1985) confirmed the earlier results for Ocean Weather Station P, stating that the increase in the amplitude of its annual CO2 cycle "reflects an increase in activity of terrestrial plants" (1985: 10,522). Contemporaneously, after two more years of data were obtained from Mauna Loa, Bacastow et al. (1985) reported that the increase in the seasonal amplitude since 1958 was "approximately 1 ppm, a sizeable fraction of the average amplitude of 6 ppm," adding that "it seems likely that the increase mainly reflects enhanced metabolic activity of the land biota" and that "one obvious factor that might produce this enhancement is the CO2 concentration itself " (1985: 10,529).

Reaffirmations of the reality of this CO2-induced phenomenon continue to appear as more and more data are collected and analyzed. Keeling (1994), for example, observed that the amplitude of the seasonal CO2 cycle increased by as much as 20 percent at high latitudes in both hemispheres between 1988 and 1993, noting that "a preliminary investigation suggests that an increase in the net primary production of plants . . . caused the amplitude increase" (1994: 110). Fourteen months later, Keeling et al. (1995) reported that the amplitude of the seasonal CO2 cycle at Mauna Loa had also risen significantly over this time period, while Okamoto et al. (1995), after analyzing seasonal CO2 amplitude trends at 17 stations stretching from the south pole to Alaska, concluded that "CO2 fertilization exists on the global scale" (1995: 206).

Shortly thereafter, Keeling et al. (1996), working with an ever-expanding data base, reported that the annual amplitude of the seasonal CO2 cycle had increased by fully 20 percent in the latitudinal vicinity of Hawaii and by 40 percent in the Arctic since the early 1960s, noting that "the amplitude increases reflect increasing assimilation of CO2 by land plants" (1996: 146). They also observed shifts in the time of occurrence of different portions of the seasonal CO2 cycle, which suggested that the vegetative growing season had lengthened by about a week during the latter part of the same time period. Then, in an analysis of reflectance data obtained from satellites deployed to monitor various processes on the earth's surface, Myneni et al. (1997) found that terrestrial vegetation between 45șN and 70șN latitudes had grown steadily more productive from 1981 to 1991 and that, simultaneously, the region's active growing season had lengthened by approximately 12 days, a development that Fung has called "the first direct observation of the biosphere that photosynthesis has increased on such a broad scale for such a long time" (1997: 659).

Productivity of plants and biodiversity
in the earth's ecosystems

The evidence for an ongoing CO2-induced rejuvenation of the biosphere that has been reviewed in the preceding pages is irrefutable: the totality of earth's plant life is growing ever more vigorously as we flood the air with ever more carbon dioxide. This development is fortunate indeed, for many of man's activities have consequences that are not nearly so benevolent and that truly do degrade earth's ecosystems, leading to massive reductions in biodiversity (Pimm et al. 1995; Vitousek et al. 1997). This one beneficent side-effect of our industrial activities, however, tends to mitigate the adverse consequences of many facets of industrialization. In some cases, the increase in the concentration of atmospheric CO2 more than compensates: it has clearly resulted in a net increase in the planet's vegetative biomass over the past several decades, as is readily evident from long- term measurements of the air's CO2 concentration and contemporary measurements of the planet's surface reflectance. Even measurements of atmospheric oxygen support this scenario (Keeling and Shertz 1992; Bender et al. 1996; Keeling et al. 1996) for, as Bender (1996) has noted, they suggest "the existence of a large oxygen source, which can only be from photosynthesis associated with the net growth of the land biosphere" (1996: 195).

This CO2-induced increase in vegetative productivity may well be one of the best allies we will ever have in our battle to preserve the planet's biodiversity; in a landmark study of the vascular plant components of 94 terrestrial ecosystems from every continent of the globe except Antarctica, it was found that biodiversity in an ecosystem is more positively correlated with its productivity than it is with anything else (Scheiner and Rey-Benayas 1994). What is more, a major review of interactions between plants and animals in 51 terrestrial ecosystems found that the biomass of plant-eating animals or herbivores was also an increasing function of above-ground primary production (McNaughton et al. 1989). A review of 22 aquatic ecosystems found that the herbivore biomass of watery habitats increased in response to a rise in underwater vegetative productivity (Cyr and Pace 1993) and a number of experiments have demonstrated that the growth of aquatic plants is also enhanced as the air's CO2 content rises (Titus et al. 1990; Raven 1991, 1993; Sand-Jensen et al. 1992; Titus 1992; Madsen 1993; Riebesell et al. 1993; Madsen and Sand-Jensen 1994; Hein and Sand-Jensen 1997; Shapiro 1997). Consequently, it is abundantly clear that earth's animal life-both terrestrial and aquatic- will respond to rising levels of atmospheric CO2 with increases in population that will parallel the increases in the plant kingdom, for "the greater the food base, the greater the superstructure of life that can be supported" (Idso 1995a: 13). Greater populations of individual organisms are clearly required for greater biodiversity, as all species must maintain a certain "critical biomass" to sustain their identities and ensure their long-term viability.

Conclusions

An increase in the concentration of atmospheric CO2 significantly stimulates the growth and development of plants while dramatically enhancing their efficient use of water. These desirable manifestations of carbon dioxide's aerial fertilization effect are rooted in fundamental properties of plants that express themselves almost universally, even in the face of significant resource deficiencies and environmental stresses. Consequently, as the carbon dioxide content of the atmosphere has risen because of the large-scale utilization of fossil fuels, so too has the productivity of the planet's vegetation risen because of the magnitude of mankind's CO2 emissions.

The striking consequences of this mutually beneficial phenomenon are evident in numerous tree-ring records, historical trends in global forest productivity, and the increasing amplitude of the atmosphere's seasonal CO2 cycle. Indeed, the on-going rise in the air's CO2 content is enhancing agricultural productivity the world over (Wittwer 1995) at the same time as it helps to sustain the biodiversity of the planet's natural ecosystems. Thus, Wittwer has written truly of this exceptional consequence of humanity's industrial activity that, "the rising level of atmospheric CO2 is a universally free premium, gaining in magnitude with time, on which we can all reckon for the future" (1997: 13).

References

Abrams, M.D., and D.A. Orwig (1995). Structure, radial growth dynamics and recent climatic variations of a 320-year-old Pinus rigida rock outcrop community. Oecologia 101: 353-360.

Amthor, J.S. (1995). Terrestrial higher-plant response to increasing atmospheric [CO2] in relation to the global carbon cycle. Global Change Biol 1: 243-274.

Arp, W.J. (1991). Effects of source-sink relations on photosynthetic acclimation to elevated CO2. Plant Cell Environ 14: 869-75.

Arp, W.J., and B.G. Drake (1991). Increased photosynthetic capacity of Scirpus olneyi after 4 years of exposure to elevated CO2. Plant Cell Environ 14: 1003-06.

Babenko, Y.S., G.I. Tyrugina, E.F. Origoreev, L.M. Dalgikh, and T.I. Borisova (1985). Biological activity and physiological biochemical properties of phosphate dissolving bacteria. Microbiol 53: 427-33.

Bacastow, R.B., C.D. Keeling, and T.P. Whorf (1985). Seasonal amplitude increase in atmospheric CO2 concentration at Mauna Loa, Hawaii, 1959-1982. J Geophys Res 90: 10,529-40.

Barton, C.V.M., H.S.J. Lee, and P.J. Jarvis (1993). A branch bag and CO2 control system for long-term CO2 enrichment of mature Sitka spruce (Picea sitchensis (Bong. Carr.). Plant Cell Environ 16: 1139-48.

Batjes, N.H., and W.G. Sombroek (1997). Possibilities for carbon sequestration in tropical and subtropical soils. Global Change Biol 3: 161-73.

Bazzaz, F.A., and E.D. Fajer (1992). Plant life in a CO2-rich world. Sci Amer (Jan): 68-74.

Becker, M. (1989). The role of climate on present and past vitality of silver fir forests in the Vosges mountains of northeastern France. Can J For Res 19: 1110-17.

Bender, M. (1996). A quickening on the uptake? Nature 381: 195-96.

Bender, M., T. Ellis, P. Tans, R. Francey, and D. Lowe (1996). Variability in the O2/N2 ratio of southern hemispheric air, 1991-1994: implications for the carbon cycle. Global Biogeochem Cycles 10: 9-21.

Berry, J., and O. Bjorkman (1980). Photosynthetic response and adaptation to temperature in higher plants. Ann Rev Plant Physiol 31: 491-543.

Bjorkdahl, G., and H. Eriksson (1989). Effects of forest decline on increment in Norway spruce (Picea abies (L.) Karst) in southern Sweden. In K. Bjor and B. Halvorsen (eds), Air pollution as stress factor in Nordic forests. Medd Norsk Inst Skogforsk 42: 19-36.

Bjorkman O., M. Badger, and P.A. Armond (1978). Thermal acclimation of photosynthesis: Effect of growth temperature on photosynthetic characteristics and components of the photosynthetic apparatus in Nerium oleander. Carnegie Inst Wash Yearbook 77: 262-76.

Bowes, G. (1993). Facing the inevitable: Plants and increasing atmospheric CO2. Ann Rev Plant Physiol Plant Mol Biol 44: 309-32.

Boyle, J.R., and G.K. Voigt (1973). Biological weathering of silicate minerals: implications for tree nutrition and soil genesis. Plant Soil 38: 191-201.

Boyle, J.R., G.K. Voigt, and B.L. Sawhney (1974). Chemical weathering of biotite by organic acids. Soil Sci 117: 42-45.

Burk, D. (1961). On the use of carbonic anhydrase in carbonate and amine buffers for CO2 exchange in manometric vessels, atomic submarines, and industrial CO2 scrubbers. Ann New York Acad Sci 92: 372-400.

Busing, R.T. (1989). A half century of change in a Great Smokey Mountain cove forest. Bull Torrey Bot Club 116: 282-88.

Campbell, W.J., L.H. Allen Jr., and G. Bowes (1988). Effects of CO2 concentration on rubisco activity, amount, and photosynthesis in soybean leaves. Plant Physiol 88: 1310-16.

Caporn, S.J.M., D.W. Hand, T.A. Mansfield, and A.R. Wellburn (1994). Canopy photosynthesis of CO2-enriched lettuce (Lactuca sativa L.). Response to short-term changes in CO2, temperature and oxides of nitrogen. New Phytol 126: 45-52.

Ceulemans, R., and M. Mousseau (1994). Effects of elevated atmospheric CO2 on woody plants. New Phytol 127: 425-46.

Chen, D.-X., M.B. Coughenour, A.K. Knapp, C.E. Owensby (1994). Mathematical simulation of C4 grass photosynthesis in ambient and elevated CO2. Ecol Modelling 73: 63-80.

Chen, J.J., and J.M. Sung (1990). Gas exchange rate and yield responses of Virginia-type peanut to carbon dioxide enrichment. Crop Sci 30: 1085-89.

Cizkova-Koncalova, H., J. Kvet, and K. Thompson (1992). Carbon starvation: a key to reed decline in eutrophic lakes. Aquatic Bot 43: 105-13.

Clarkson, D.T. (1985). Factors affecting mineral nutrient acquisition by plants. Ann Rev Plant Physiol 36: 77-115.

Clement, C.R., M.J. Hopper, L.H.P. Jones, and E.L. Leafe (1978). The uptake of nitrate by Lolium perenne from flowering nutrient solution. II. Effect of light, defoliation, and relationship to CO2 flux. J Exp Bot 29: 1173-83.

Cleveland, W.S., A.E. Frenny, and T.E. Graedel (1983). The seasonal component of atmospheric CO2: information from new approaches to the decomposition of seasonal time-series. J Geophys Res 88: 10,934-40.

Conroy, J. (1989). Influence of high CO2 on Pinus radiata. PhD thesis, Macquarie University, Australia.

Cure, J.D., and B. Acock (1986). Crop responses to carbon dioxide doubling: a literature survey. Agric For Meteorol 8: 127-45.

Curtis, P.S., L.M. Balduman, B.G. Drake, and D.F. Whigham (1990). Elevated atmospheric CO2 effects on below ground processes in C3 and C4 estuarine marsh communities. Ecology 71: 2001-06.

Curtis, P.S., D.R. Zak, K.S. Pregitzer, and J.A. Terri (1994). Above- and below-ground response of Populus grandidentata to elevated atmospheric CO2 and soil N availability. Plant Soil 165: 45-51.

Cyr, H., and M.L. Pace (1993). Magnitude and patterns of herbivory in aquatic and terrestrial ecosystems. 361: 148-50.

Davis, M.B. (1989). Lags in vegetation response to greenhouse warming. Climatic Change 15: 75-82.

De Jong, T.M., B.G. Drake, and R.W. Pearcy (1982). Gas exchange responses of Chesapeake Bay tidal marsh species under field and laboratory conditions. Oecologia 52: 5-11.

Delucia, E.H., T.W. Sasek, and B.R. Strain (1985). Photosynthetic inhibition after long-term exposure to elevated levels of atmospheric carbon dioxide. Photosyn Res 7: 175-84.

Dobson, A. (1992). Withering heats: global warming will exact heavy toll on earth's biodiversity. Nat Hist 101, 9: 2-8.

Drake, B.G. (1989). Photosynthesis of salt marsh species. Aquatic Bot 34: 167-80.

--- (1992a). The impact of rising CO2 on ecosystem production. Water Air Soil Poll 64: 25-44.

--- (1992b). Global warming: the positive impact of rising carbon dioxide levels. Eco-Logic 1, 3: 20-22.

--- (1992c). A field study of the effects of elevated CO2 on ecosystem processes in a Chesapeake Bay wetland. Aust J Bot 40: 579-95.

Drake B.G., and P.W. Leadley (1991). Canopy photosynthesis of crops and native plant communities exposed to long-term elevated CO2. Plant Cell Environ 14: 853-60.

Dufrene, E., J.-Y. Pontailler, and B. Saugier (1993). A branch bag technique for simultaneous CO2 enrichment and assimilation measurements on beech (Fagus sylvatica L.). Plant Cell Environ 16: 1131-38.

Dugas, W.A., and P.J. Pinter, Jr. (1994). The free-air carbon dioxide enrichment (FACE) cotton project: a new field approach to assess the biological consequences of global change. Agric For Meteorol 70: 1-342.

Dyer, J.M. (1995). Assessment of climatic warming using a model of forest species migration. Ecol Modelling 79: 199-219.

Edwards, C.A. (1988). Earthworms and agriculture. Agron Abstr 80: 274.

--- (1997). Earthworm Ecology. Boca Raton, FL: St. Lucie Press.

Eichkorn, T. (1986). Wachstumanalysen an Fichten in Sudwestdeutschland. Allg Forst Jagdztg 157: 125-39.

Falkengren-Grerup, U., and H. Eriksson (1990). Changes in soil, vegetation and forest yield between 1947 and 1988 in beech and oak sites of southern Sweden. For Ecol Manage 38: 37-53.

Field, C.B. (1994). Arctic chill for CO2 uptake. Nature 371: 472-73.

Fiscus, E.L., C.D. Reid, J.E. Miller, and A.S. Heagle (1997). Elevated CO2 reduces O3 flux and O3-induced yield losses in soybeans: possible implications for elevated CO2 studies. J Exp Bot 48: 307-13.

Faria, T., D. Wilkins, R.T. Besford, M. Vaz, J.S. Pereira, and M.M. Chaves (1996). Growth at elevated CO2 leads to down-regulation of photosynthesis and altered response to high temperature in Quercus suber L. seedlings. J Exp Bot 47: 1755-61.

Finn, G.A., and W.A. Brun (1982). Effect of atmospheric CO2 enrichment on growth, nonstructural carbohydrate content, and root nodule activity in soybean. Plant Physiol 69: 327-31.

Fogel, R. (1983). Root turnover and productivity of forests. Plant Soil 71: 75-85.

Fung, I. (1997). A greener north. Nature 386: 659-60.

Gear, A.J.,and B. Huntley (1991). Rapid changes in the range limits of Scots pine 4000 years ago. Science 251: 544-47.

Gebauer, R.L.E., J.F. Reynolds, B.R. Strain (1996). Allometric relations and growth in Pinus taeda: the effect of elevated CO2 and changing N availability. New Phytol 134: 85-93.

Gifford, R.M. (1992). Interaction of carbon dioxide with growth-limiting environmental factors in vegetative productivity: implications for the global carbon cycle. Adv Bioclim 1: 24-58.

Glatzel, G., M. Kazda, D. Grill, G. Halbwachs, and K. Katzensteiner (1987). Ernahrungsstorungen bei Fichte als Komplexwirkung von Nadelschaden und erhohter Stickstoffdeposition-ein Wirkungsmechanismus des Waldsterbens? Allg Forst Jagdztg 158: 91-97.

Goodfellow, J., D. Eamus, and G. Duff (1997). Diurnal and seasonal changes in the impact of CO2 enrichment on assimilation, stomatal conductance and growth in a long-term study of Mangifera indica in the wet-dry tropics of Australia. Tree Physiol 17: 291-99.

Gore, A. (1992). Earth in the balance: ecology and the human spirit. Boston: Houghton Mifflin.

Graham, R.C., H.B. Wood, and M.A. Lueking (1988). Soil morphologic development in a 40-year-old chaparral biosequence. Agron Abstr 80: 258.

Graumlich, L.J., L.B. Brubaker, and C.C. Grier (1989). Long-term trends in forest net primary productivity: Cascade Mountains, Washington. Ecology 70: 405-10.

Graybill, D.A. (1987). A network of high elevation conifers in the western US for detection of tree-ring growth response to increasing atmospheric carbon dioxide. In G.C. Jacoby Jr., and J. W. Hornbeck (eds), Proceedings of the international symposium on ecological aspects of tree-ring analysis (Washington, DC: US Dept. of Energy): 463-74.

Graybill, D.A., and S.B. Idso (1993). Detecting the aerial fertilization effect of atmospheric CO2 enrichment in tree-ring chronologies. Global Biogeochem Cycles 7: 81-95.

Grulke, N.E., G.H. Riechers, W.C. Oechel, U. Hjelm, and C. Jaeger (1990). Carbon balance in tussock tundra under ambient and elevated atmospheric CO2. Oecologia 83: 485-94.

Gunderson, C.A., R.J. Norby, and S.D. Wullschleger (1993). Foliar gas exchange responses of two deciduous hardwoods during three years of growth in elevated CO2: no loss of photosynthetic enhancement. Plant Cell Environ 16: 797-807.

Gunderson, C.A.,and S.D. Wullschleger (1994). Photosynthetic acclimation in trees to rising atmospheric CO2: a broader perspective. Photosyn Res 39: 369-88.

Hardy, R.W.F., and U.D. Havelka (1973). Symbiotic N2 fixation: multifold enhancement by CO2-enrichment of field-grown soybeans. Plant Physiol Supplement 48: 35.

--- (1975). Photosynthate as a major factor limiting nitrogen fixation by field-grown legumes with emphasis on soybeans. In P.S. Nutman (ed), Symbiotic Nitrogen Fixation in Plants (Cambridge: Cambridge University Press: 421-39.

Hardy, R.W.F., U.D. Havelka, and B. Quebedeaux (1976). Opportunities for improved seed yield and protein production: N2 fixation, CO2 fixation, and O2 control of reproductive growth. In National Research Council (eds), Genetic Improvement of Seed Protein (Washington, DC: National Academy Press): 196-228.

--- (1978). The opportunity for and significance of alteration of ribulose 1,5-bisphosphate carboxylase activities in crop production. In H.W. Siegelman and G. Hind (eds), Photosynthetic Carbon Assimilation (New York: Plenum): 165-78.

Hari, P., and H. Arovaara (1988). Detecting CO2 induced enhancement in the radial increment of trees. Evidence from the northern timberline. Scand J For Res 3: 67-74.

Hari, P., H. Arovaara, T. Raunemaa, and A. Hautojarvi (1984). Forest growth and the effects of energy production: a method for detecting trends in the growth potential of trees. Can J For Res 14: 437-40.

Harley, P.C., J.D. Tenhunen, O.L. Lange (1986). Use of an analytical model to study the limitations on net photosynthesis in Arbutus unedo under field conditions. Oecologia 70: 393-401.

Havelka, U.D., R.W.F. Hardy (1976). Legume N2 fixation as a problem in carbon nutrition. In W.E. Newton and C.J. Nyman (eds), Proceedings of the 1st Symposium on Nitrogen Fixation, Vol. 2. (Pullman, WA: Washington State University Press): 456-75.

Hein, M., and S, Sand-Jensen (1997). CO2 increases oceanic primary production. Nature 388: 526-27.

Hendrey, G.R., K.F. Lewin, and J. Nagy (1993). Free air carbon dioxide enrichment: Development, progress, results. Vegetatio 104/105: 17-31.

Henning, F.P., C.W. Wood, H.H. Rogers, G.B. Runion, and S.A. Prior (1996). Composition and decomposition of soybean and sorghum tissues grown under elevated atmospheric carbon dioxide. J Environ Qual 25: 822-27.

Hogan, K.P., A.P. Smith, L.H. Ziska (1991). Potential effects of elevated CO2 and changes in temperature on tropical plants. Plant Cell Environ 14: 763-78.

Hornbeck, J.W. (1987). Growth patterns of red oak and red and sugar maple relative to atmospheric decomposition. In Proceedings of the 16th Central Hardwood Forest Conference (Knoxville, TN: University of Tennessee): 277-82.

Hornbeck, J.W., R.B. Smith, and C.A. Federer (1988). Growth trends in 10 species of trees in New England, 1950-1980. Can J For Res 18: 1337-40.

Hungate, B.A., E.A. Holland, R.B. Jackson, F.S. Chapin III, H.A. Mooney, and C.B. Field (1997). The fate of carbon in grasslands under carbon dioxide enrichment. Nature 388: 576-79.

Intergovernmental Panel on Climate Change (IPCC) (1990). Climate Change: The IPCC Scientific Assessment. Report prepared for IPCC by Working Group I. John T. Houghton et al. (eds). Cambridge: Cambridge University Press.

Intergovernmental Panel on Climate Change, Working Group I (IPCC I) (1996). Climate Change 1995: The Science of Climate Change. Contribution of Working Group I to the Second Assessment Report of the Intergovernmental Panel on Climate Change. John T. Houghton et al. (eds). Cambridge: Cambridge University Press.

Idso, K.E. (1992a). Plant responses to rising levels of atmospheric carbon dioxide: A compilation and analysis of the results of a decade of international research into the direct biological effects of atmospheric CO2 enrichment. Tempe, AZ: Office of Climatology, Arizona State University.

--- (1995a). Rising CO2: a breath of new life for the biosphere. World Climate Rev 3(3): 8-15.

Idso, K.E., and S.B. Idso (1994). Plant responses to atmospheric CO2 enrichment in the face of environmental constraints: A review of the past 10 years' research. Agric For Meteorol 69: 153-203.

Idso, S.B. (1989a). Carbon Dioxide: Friend or Foe? Tempe, AZ: IBR Press.

--- (1989b). Carbon dioxide, soil moisture, and future crop production. Soil Sci 147: 305-07.

--- (1991a). Cooling the global greenhouse? The World and I 6, 3: 276-83.

--- (1991b). Carbon dioxide and the fate of Earth. Global Environ Change 1: 178-82.

--- (1992b). Carbon dioxide and global change: end of nature or rebirth of the biosphere? In J.H. Lehr (ed), Rational Readings on Environmental Concerns (New York: Van Nostrand Reinhold): 414-33.

--- (1995b). CO2 and the Biosphere: The Incredible Legacy of the Industrial Revolution. St. Paul, MN: Department of Soil, Water and Climate, University of Minnesota.

--- (1997). The poor man's biosphere, including simple techniques for conducting CO2 enrichment and depletion experiments on aquatic and terrestrial plants. Environ Exp Bot: in press

Idso, S.B., S.G. Allen, M.G. Anderson, and B.A. Kimball (1989). Atmospheric CO2 enrichment enhances survival of Azolla at high temperatures. Environ Exp Bot 29: 337-41.

Idso, S.B., K.E. Idso, R.L. Garcia, B.A. Kimball, and J.K. Hoober (1995). Effects of atmospheric CO2 enrichment and foliar methanol application on net photosynthesis of sour orange tree (Citrus aurantium; Rutacea) leaves. Amer J Bot 82: 26-30.

Idso, S.B., and B.A. Kimball (1991a). Effects of two and a half years of atmospheric CO2 enrichment on the root density distribution of three-year-old sour orange trees. Agric For Meteorol 55: 345-49.

--- (1991b). Downward regulation of photosynthesis and growth at high CO2 levels: no evidence for either phenomenon in three-year study of sour orange trees. Plant Physiol 96: 990-92.

--- (1992b). Seasonal fine-root biomass development of sour orange trees grown in atmospheres of ambient and elevated CO2 concentration. Plant Cell Environ 15: 337-41.

--- (1997). Effects of long-term atmospheric CO2 enrichment on the growth and fruit production of sour orange trees. Global Change Biol 3: 89-96.

Idso, S.B., B.A. Kimball, and S.G. Allen (1991). CO2 enrichment of sour orange trees: two-and-a-half years into a long-term experiment. Plant Cell Environ 14: 351-53.

Idso, S.B., B.A. Kimball, and J.R. Mauney (1988). Effects of atmospheric CO2 enrichment on root:shoot ratios of carrot, radish, cotton and soybean. Agric Ecosys Environ 22: 293-99.

Idso, S.B., and J.A. Quinn (1983). Vegetational Redistribution in Arizona and New Mexico in Response to a Doubling of the Atmospheric CO2 Concentration. Tempe, AZ: Climatology Laboratory , Arizona State University.

Ineichen, K., V. Wiemken, and A. Wiemken (1995). Shoots, roots, and ectomycorrhiza of pine seedlings at elevated atmospheric carbon dioxide. Plant Cell Environ 18: 703-07.

Innes, J.L., and E.R. Cook (1989). Tree-ring analysis as an aid to evaluating the effects of pollution on tree growth. Can J For Res 19: 1174-89.

Jackson, W.A., R.J. Volk, and D.W. Israel (1980). Energy supply and nitrate assimilation in root systems. In A. Tanaka (ed), Carbon-nitrogen Interaction in Crop Production (Tokyo: Japanese Society for Promotion of Science): 25-40.

Jacob, J., C. Greitner, and B.G. Drake (1995). Acclimation of photosynthesis in relation to Rubisco and non-structural carbohydrate contents and in situ carboxylase activity in Scirpus olneyi grown at elevated CO2 in the field. Plant Cell Environ 18: 875-84.

Jacoby, G.C. (1986). Long-term temperature trends and a positive departure from the climate- growth response since the 1950s in high elevation lodgepole pine from California. In C. Rosenzweig and R. Dickinson (eds), Proceedings of the NASA Conference on Climate-Vegetation Interactions (Boulder, CO: University Corporation for Atmospheric Research): 81-83.

Johnson, D.L. (1988). Biomantle evolution and the redistribution of earth materials and artifacts. Agron Abstr 80: 259.

Johnson, H.B., H.W. Polley, and H.S. Mayeux (1993). Increasing CO2 and plant-plant interactions: effects on natural vegetation. Vegetatio 104/105: 157-70.

Johnston, M.C. (1963). Past and present grasslands of southern Texas and northeastern Mexico. Ecology 44: 456-66.

Jones, M.B., J.C. Brown, A. Raschi, and F. Miglietta (1995). The effects on Arbutus unedo L. of long- term exposure to elevated CO2. Global Change Biol 1: 295-302.

Jongen, M., M.B. Jones, T. Hebeisen, H. Blum, and G. Hendrey (1995). The effects of elevated CO2 concentrations on the root growth of Lolium perenne and Trifolium repens grown in a FACE system. Global Change Biol 1: 361-71.

Jozsa, L.A., and J. M. Powell (1987). Some climatic aspects of biomass productivity of white spruce stem wood. Can J For Res 17: 1075-79.

Jurik, T.W., J.A. Weber, and D.M. Gates (1984). Short-term effects of CO2 on gas exchange of leaves of bigtooth aspen (Populus grandidentata) in the field. Plant Physiol 75: 1022-26.

Kapulnik, Y., R. Gafny, and Y. Okon (1983). Effect of Azospirillum spp. inoculation development and NO3- uptake in wheat (Triticum aestivum cv. Miriam) in hydroponic system. Can J Bot 63: 627-31.

Kauppi, P.E., K. Mielikainen, K. Kuusela (1992). Biomass and carbon budget of European forests, 1971-1990. Science 256: 70-74.

Keeling, C.D. (1994). A study of the abundance and 13C/12C ratio of atmospheric carbon dioxide and oceanic carbon in relation to the global carbon cycle. In M.R. Riches (ed), Global Change Research: Summaries of Research in FY 1994. (Washington, DC: US Department of Energy): 109-10.

Keeling, C.D., J.F.S. Chin, and T.P. Whorf (1996). Increased activity of northern hemispheric vegetation inferred from atmospheric CO2 measurements. Nature 382: 146-49.

Keeling, C.D., T.P. Whorf, M. Wahlen, and J. van der Pilcht (1995). Interannual extremes in the rate of rise of atmospheric carbon dioxide since 1980. Nature 375: 666-70.

Keeling, C.D., T.P. Whorf, C.S. Wong, R.D. Bellagay (1985). The concentration of carbon dioxide at ocean weather station P from 1969-1981. J Geophys Res 90: 10,511-28

Keeling, R., S.C. Piper, M. Heimann (1996). Global and hemispheric CO2 sinks deduced from changes in atmospheric O2 concentration. Nature 381: 218-21.

Keeling, R., amd S. Shertz (1992). Seasonal and interannual variations in atmospheric oxygen and implications for the global carbon cycle. Nature 358: 723-27.

Kellomaki, S., and K.-Y. Wang (1996). Photosynthetic responses to needle water potentials in Scots pine after a four-year exposure to elevated CO2 and temperature. Tree Physiol 16: 765-72.

Kenk, G. (1989). Zuwachsuntersuchungen im zusammenhang mit den gegenwartigen waldschaden in Baden-WŸrttemberg. In J.B. Bucher and W.I. Bucher (eds), Air pollution and forest decline (Brimensdorf, Switzerland: Eidgenossische Anstalt fŸr das forstliche Versuchswesen): 263-69.

Kenk, G, and H. Fischer (1988). Evidence from nitrogen fertilization in the forests of Germany. Environ Poll 54: 199-218.

Kienast, F.,and R.J. Luxmoore (1988). Tree-ring analysis and conifer growth responses to increased atmospheric CO2 levels. Oecologia 76: 487-95.

Kimball, B.A. (1983a). Carbon dioxide and agricultural yield: an assemblage and analysis of 430 prior observations. Agron J 75: 779-88.

--- (1983b). Carbon Dioxide and Agricultural Yield: An Assemblage and Analysis of 770 Prior Observations. Phoenix, AZ: US Water Conservation Laboratory.

Kimball, B.A., and S.B. Idso (1983). Increasing atmospheric CO2: effects on crop yield, water use and climate. Agric Water Management 7: 55-72.

King, A.W., W.M. Post, and S.D. Wullschleger (1997). The potential response of terrestrial carbon storage to changes in climate and atmospheric CO2. Climatic Change 35: 199-227.

King, J.S., R.B. Thomas, and B.R. Strain (1996). Growth and carbon accumulation in root systems of Pinus taeda and Pinus ponderosa seedlings as affected by varying CO2, temperature and nitrogen. Tree Physiol 16: 635-42.

Kirschbaum, M.U.F. (1994). The sensitivity of C3 photosynthesis to increasing CO2 concentration: a theoretical analysis of its dependence on temperature and background CO2 concentration. Plant Cell Environ 17: 747-54.

Koch, G.W., and H.A. Mooney (1996a). Carbon Dioxide and Terrestrial Ecosystems. San Diego, CA: Academic Press.

--- (1996b). Response of terrestrial ecosystems to elevated CO2: a synthesis and summary. In Koch and Mooney 1996a: 415-29.

Kramer, P.J. (1981). Carbon dioxide concentration, photosynthesis and dry matter production. BioSci 31: 29-34.

Kubiske, M.E., and K.S. Pregitzer (1996). Effects of elevated CO2 and light availability on the photosynthetic light response of trees of contrasting shade tolerance. Tree Physiol 16: 351-58.

Kubiske, M.E., and K.S. Pregitzer (1997). Ecophysiological responses to simulated canopy gaps of two tree species of contrasting shade tolerance in elevated CO2. Functional Ecol 11: 24-32.

Kubiske, M.E., K.S. Pregitzer, C.J. Mikan, D.R. Zak, J.L. Maziasz, and J.A. Teeri (1997). Populus tremuloides photosynthesis and crown architecture in response to elevated CO2 and soil N availability. Oecologia 110: 328-36.

LaMarche, V.C., Jr., D.A. Graybill, H.C. Fritts, and M.R. Rose (1984). Increasing atmospheric carbon dioxide: tree ring evidence for growth enhancement in natural vegetation. Science 223: 1019-21.

Lamborg, M.R., R.W. Hardy, and E.A. Paul (1983). Microbial effects. In E.R. Lemon (ed). CO2 and Plants: The Response of Plants to Rising Levels of Atmospheric Carbon Dioxide (Boulder, CO: Westview Press): 131-76.

Lawlor, D.W., R.A.C. Mitchell (1991). The effects of increasing CO2 on crop photosynthesis and productivity: a review of field studies. Plant Cell Environ 14: 807-18.

Lekkerkerk, L.J.A., J.A. Van Veen, S.C. Van de Geijn (1990). Influence of climatic change on soil quality; consequences of increased atmospheric CO2-concentration on carbon input and turnover in agro-ecosystems. In J. Goudriaan, H. Van Keulen, and H.H. Van Laar (eds). The Greenhouse Effect and Primary Productivity in European Agro-ecosystems (Wageningen, NL: Pudoc): 46-47.

Lemon, E.R. (1983). CO2 and Plants: The Response of Plants to Rising Levels of Atmospheric Carbon Dioxide. Boulder, CO: Westview Press.

Lewis, J.D., K.L. Griffin, R.B. Thomas, and B.R. Strain (1994). Phosphorus supply affects the photosynthetic capacity of loblolly pine grown in elevated carbon dioxide. Tree Physiol 14: 1229-44.

Liang, N., and K. Maruyama (1995). Interactive effects of CO2 enrichment and drought stress on gas exchange and water-use efficiency in Alnus firma. Environ Exp Bot 35: 353-61.

Liang, N., K. Maruyama, and Y. Huang (1996). Effects of CO2 concentration on the photosynthetic and carboxylation efficiencies of Fagus crenata and Quercus crispula. Photosynthetica 32: 355-65.

Liu, S., and R.O. Teskey (1995). Responses of foliar gas exchange to long-term elevated CO2 concentrations in mature loblolly pine trees. Tree Physiol 15: 351-59.

Long, S.P. (1991). Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: has its importance been underestimated? Plant Cell Environ 14: 729-39.

Long, S.P., B.G. Drake (1991). Effect of the long-term elevation of CO2 concentration in the field on the quantum yield of photosynthesis of the C3 sedge, Scirpus olneyi. Plant Physiol 96: 221-26.

Lowe, R.H., and H.J. Evans (1962). Carbon dioxide requirement for growth of legume nodule bacteria. Soil Sci 94: 351-56.

Luo, Y., C.B. Field, and H.A. Mooney (1994). Predicting responses of photosynthesis and root fraction to elevated [CO2]a: interactions among carbon, nitrogen, and growth. Plant Cell Environ 17: 1195-204.

Luxmoore, R.J., E.G. O'Neill, J.M. Ells, H.H. Rogers (1986). Nutrient-uptake and growth responses of Virginia pine to elevated atmospheric CO2. J Environ Qual 15: 244-51.

MacDowall, F.D.H. (1983). Effects of light intensity and CO2 concentration on the kinetics of 1st month growth and nitrogen fixation of alfalfa. Can J Bot 61: 731-40.

Madsen, T.V. (1993). Growth and photosynthetic acclimation by Ranunculus aquatilis L. in response to inorganic carbon availability. New Phytol 125: 707-15.

Madsen, T.V., and K. Sand-Jensen (1994). The interactive effects of light and inorganic carbon on aquatic plant growth. Plant Cell Environ 17: 955-62.

Marek, M.V., and J. Kalina (1996). Comparison of two experimental approaches used in the investigations of the long-term effects of elevated CO2 concentration. Photosynthetica 32: 129-33.

Maruyama, L.K., and Y. Huang (1966). Effects of CO2 concentration on the photosynthetic and carboxylation efficiencies of Fagus crenata and Quercus crispula. Photosynthetica 32: 355-65.

Masle, J., G.D. Farquhar, and R.M. Gifford (1990). Growth and carbon economy of wheat seedlings as affected by soil resistance to penetration and ambient partial pressure of CO2. Aust J Plant Physiol 17: 465-87.

McKee, I.F., J.F. Bullimore, and S.P. Long (1997). Will elevated CO2 concentrations protect the yield of wheat from O3 damage? Plant Cell Environ 20: 77-84.

McMurtrie, R.E., H.N. Comins, M.U.F. Kirschbaum, and Y.-P. Wang (1992). Modifying existing forest growth models to take account of effects of elevated CO2. Aust J Bot 40: 657-77.

McMurtrie, R.E., and Y.-P. Wang (1993). Mathematical models of the photosynthetic response of tree stands to rising CO2 concentrations and temperatures. Plant Cell Environ 16: 1-13.

McNaughton, S.J., M. Oesterheld, D.A. Frank, and K.J. Williams (1989). Ecosystem-level patterns of primary productivity and herbivory in terrestrial habitats. Nature 341: 142-44.

Micallef, B.J., P.J. Vanderveer, snf T.D. Sharkey (1996). Responses to elevated CO2 of Flaveria linearis plants having a reduced activity of cytosolic fructose-1,6-bisphosphatase. Plant Cell Environ 19: 10-16.

Molla, M.A.Z., A.A. Chowdhary, and A.H. Islam (1984). Microbial mineralization of organic phosphate in soil. Plant Soil 78: 393-99.

Morison, J.I.L. (1985). Sensitivity of stomata and water use efficiency to high CO2. Plant Cell Environ 8: 467-74.

Mortensen, L.M. (1987). Review: CO2 enrichment in greenhouses. Crop responses. Sci Hort 33: 1-25.

Mulholland, B.J., J. Craigon, C.R. Black, J.J. Colls, J. Atherton, and G. Landon (1997). Effects of elevated carbon dioxide and ozone on the growth and yield of spring wheat (Triticum aestivum L.) J Exp Bot 48: 113-22.

Murphy, P.M. (1986). Effect of light and atmospheric carbon dioxide concentration on nitrogen fixation by herbage legumes. Plant Soil 95: 399-409.

Myneni, R.B., C.D. Keeling, C.J. Tucker, G. Asrar, and R.R. Nemani (1997). Increased plant growth in the northern high latitudes from 1981 to 1991. Nature 386: 698-702.

Nie, G.Y., S.P. Long, R.L. Garcia, B.A. Kimball, R.L. LaMorte, P.J. Pinter, Jr., G.W. Wall, and A.N. Weber (1995). Effects of free-air CO2 enrichment on the development of the photosynthetic apparatus in wheat, as indicated by changes in leaf proteins. Plant Cell Environ 18: 855-64.

Nijs, I., I. Impens (1996). Effects of elevated CO2 concentration and climate-warming on photosynthesis during winter in Lolium perenne. J Exp Bot 47: 915-24.

Nilsen, S., K. Hovland, C. Dons, and S.P. Sletten (1983). Effect of CO2 enrichment on photosynthesis, growth and yield of tomato. Sci Hort 20: 1-14.

Norby, R.J. (1994). Issues and perspectives for investigating root responses to elevated atmospheric carbon dioxide. Plant Soil 165: 9-20.

Norby, R.J. (1997). Inside the black box. Nature 388: 522-23.

Norby, R.J., C.A. Gunderson, S.D. Wullschleger, E.G. O'Neill, and M.K. McCracken (1992). Productivity and compensatory responses of yellow-poplar trees in elevated CO2. Nature 357: 322-24.

Norby, R.J., and E.G. O'Neill (1991). Leaf area compensation and nutrient interactions in CO2-enriched seedlings of yellow-poplar (Liriodendron tulipifera L.). New Phytol 117: 515-28.

Norby, R.J., E.G. O'Neill, and R.J. Luxmoore (1986). Effects of atmospheric CO2 enrichment on the growth and mineral nutrition of Quercus alba seedlings in nutrient-poor soil. Plant Physiol 82: 83-89.

Oechel, W.C., S. Cowles, N. Grulke, S.J. Hastings, B. Lawrence, T. Prudhomme, G. Riechers, B. Strain, D. Tissue, and G. Vourlitis (1994). Transient nature of CO2 fertilization in Arctic tundra. Nature 371: 500-03.

Oechel, W.C., and B.R. Strain (1985). Native species responses to increased atmospheric carbon dioxide concentration. In B.R. Strain, and J.D. Cure (eds), Direct Effects of Increasing Carbon Dioxide on Vegetation (Washington, DC: US Department of Energy): 117-54.

Okamoto, K., S. Tanimoto, and K. Okano (1995). Statistical analysis of the increase in atmospheric CO2 concentrations and its relation to the possible existence of CO2 fertilization of a global scale. Tellus 47B: 206-11.

Ortuno, A., A. Hermansarz, J. Noguera, V. Morales, and T. Armero (1978). Phosphorus solubilizing effect of A. niger and Pseudomonas fluorescens. Microbiol Esp 30: 113-20.

Osborne, C.P., B.G. Drake, J. LaRoche, S.P. Long (1997). Does long-term elevation of CO2 concentration increase photosynthesis in forest floor vegetation? Plant Physiol 114: 337-44.

Overpeck, J.T., P.J. Bartlein, and T. Webb III (1991). Potential magnitude of future vegetation change in eastern North America: comparisons with the past. Science 254: 692-95.

Owensby, C.E., J.M. Ham, A.K. Knapp, C.W. Rice, P.I. Coyne, and L.M. Auen (1996). Ecosystem-level responses of tallgrass prairie to elevated CO2. In G.W. Koch and H.A. Mooney (eds), Carbon Dioxide and Terrestrial Ecosystems (San Diego, CA: Academic Press): 175-93.

Paine, S. (1988). No escape from the global greenhouse. New Sci 1638: 38-43.

Pallas, J.E. (1965). Transpiration and stomatal opening with changes in carbon dioxide content of the air. Science 147: 171-73.

Parker, M.L. (1987). Recent abnormal increase in tree-ring widths: a possible effect of elevated atmospheric carbon dioxide. In G.C. Jacoby, Jr. and J.W. Hornbeck (eds), Proceedings of the International Symposium on Ecological Aspects of Tree-ring Analysis (Washington, DC: US Department of Energy): 511-21.

Pearcy, R.W., and O. Bjorkman (1983). Physiological effects. In E.R. Lemon (ed), CO2 and Plants: The Response of Plants to Rising Levels of Atmospheric Carbon Dioxide (Boulder, CO: Westview Press): 65-105.

Pearman, G.I., and P. Hyson (1981). The annual variation of atmospheric CO2 concentration observed in the northern hemisphere. J Geophys Res 86: 9839-43.

Percival, D.C., J.T.A. Proctor, and M.J. Tsujita (1996). Whole-plant net CO2 exchange of raspberry as influenced by air and root-zone temperature, CO2 concentration, irradiation, and humidity. J Amer Soc Hort Sci 121: 838-45.

Peters, R.L., and J.D.S. Darling (1985). The greenhouse effect and nature reserves. BioSci 35: 707-17.

Phillips, D.A., K.D. Newell, S.A. Hassel, and C.E. Felling (1976). The effect of CO2 enrichment on root nodule development and symbiotic N2 reduction in Pisum sativum L. Amer J Bot 63: 356-62.

Phillips, O.L., and A.H. Gentry (1994). Increasing turnover through time in tropical forests. Science 263: 954-58.

Pimm, S.L., G.J. Russell, J.L. Gittleman, and T.M. Brooks (1995). The future of biodiversity. Science 269: 347-50.

Pimm, S.L., and A.M. Sugden (1994). Tropical diversity and global change. Science 263: 933-34.

Pinter, P.J. Jr., B.A. Kimball, R.L. Garcia, G.W. Wall, D.J. Hunsaker, and R.L. LaMorte (1996). Free-air CO2 enrichment: responses of cotton and wheat crops. In G.W. Koch, and H.A. Mooney (eds), Carbon Dioxide and Terrestrial Ecosystems (San Diego, CA: Academic Press): 215-49.

Pitelka, L.F., R.H. Gardner, J. Ash, S. Berry, H. Gitay, I.R. Noble, A. Saunders, R.H.W. Bradshaw, L. Brubaker, J.S. Clark, M.B. Davis, S. Sugita, J.M. Dyer, R. Hengeveld, G. Hope, B. Huntley, G.A. King, S. Lavorel, R.N. Mack, G.P. Malanson, M. McGlone, I.C. Prentice, and M. Rejmanek (1997). Plant migration and climate change. Amer Sci 85: 464-73.

Pitman, M. (1977). Ion transport into the xylem. Ann Rev Plant Physiol 28: 71-88.

Polley, H.W., H.B. Johnson, H.S. Mayeux, C.R. Tischler, and D.A. Brown (1996). Carbon dioxide enrichment improves growth, water relations and survival of droughted honey mesquite (Prosopis glandulosa) seedlings. Tree Physiol 16: 817-23.

Poorter, H. (1993). Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. Vegetatio 104/105: 77-97.

Possingham, H.P. (1993). Impact of elevated atmospheric CO2 on biodiversity: mechanistic population-dynamic perspective. Aust J Bot 41: 11-21.

Pregitzer, K.S., D.R. Zak, P.S. Curtis, M.E. Kubiske, J.A. Teeri, C.S. Vogel (1995). Atmospheric CO2, soil nitrogen and turnover of fine roots. New Phytol 129: 579-85.

Pretzsch, H. (1985a). Wachstumsmerkmale suddeutscher Kiefernbestande in den letzen 25 Jahren. Forschungsbericht der Forstlichen Forschungs-Anstalt Munchen 65.

--- (1985b). Wachstumsmerkmale oberpfalzischer Kiefernbestande in den letzten 30 Jahren. Vitalitatszustand-Strukturverhaltnisse-Zuwachsgang. Allg Forstzeitschr 42: 1122-26.

Prior, S.A., H.H. Rogers, G.B. Runion, B.A. Kimball, J.R. Mauney, K.F. Lewin, J. Nagy, and G.R. Hendrey (1995). Free-air carbon dioxide enrichment of cotton: Root morphological characteristics. J Environ Qual 24: 678-83.

Prior, S.A., H.A. Torbert, G.B. Runion, H.H. Rogers, C.W. Wood, B.A. Kimball, R.L. LaMorte, P.J. Pinter, and G.W. Wall (1997). Free-air carbon dioxide enrichment of wheat: soil carbon and nitrogen dynamics. J Environ Qual 26: 1161-66.

Quebedeaux, B., U.D. Havelka, K.L. Livak, R.W.F. Hardy (1975). Effect of altered pO2 on the aerial part of soybean on symbiotic N2 fixation. Plant Physiol 56: 761-64.

Radin, J.W., B.A. Kimball, D.L. Hendrix , and J.R. Mauney (1987). Photosynthesis of cotton plants exposed to elevated levels of carbon dioxide in the field. Photosyn Res 12: 191-203.

Raven, J.A. (1991). Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: relation to increased CO2 and temperature. Plant Cell Environ 14: 779-94.

--- (1993). Phytoplankton: limits on growth rates. Nature 361: 209-10.

Reining, E. (1994). Acclimation of C3 photosynthesis to elevated CO2: hypotheses and experimental evidence. Photosynthetica 30: 519-25.

Riebesell, U., D.A. Wolf-Gladrow, and V. Smetacek (1993). Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361: 249-51.

Robinson, J.M. (1994). Speculations on carbon dioxide starvation, Late Tertiary evolution of stomatal regulation and floristic modernization. Plant Cell Environ 17: 345-54.

Roden, J.S., and M.C. Ball (1996). The effect of elevated [CO2] on growth and photosynthesis of two eucalyptus species exposed to high temperatures and water deficits. Plant Physiol 111: 909-19.

Rogers, H.H., L.H. Allen, Jr, B.A. Kimball, S.B. Idso, J.E. Miller, S.L. Rawlins, and R.C. Dahlman (1992). Potential impacts of climate change on agricultural production. Testimony before public hearing of the Committee of Enquiry on Protecting the Earth's Environment (17-18 February). Enquete Kommission, Deutcher Bundestag, Bundeshaus, Bonn, D.

Rogers, H.H., C.M. Peterson, J.N. McCrimmon, and J.D. Cure (1992). Response of plant roots to elevated atmospheric carbon dioxide. Plant Cell Environ 15: 749-52.

Rogers, H.H., G.B. Runion, and S.V. Krupa (1994). Plant responses to atmospheric CO2 enrichment with emphasis on roots and the rhizosphere. Environ Poll 83: 155-89.

Root, T.L., and S.H. Schneider (1993). Can large-scale climatic models be linked with multiscale ecological studies? Conserv Biol 7: 256-70.

Rowland, A.J., J.T. Baker, L.H. Allen, Jr., and G. Bowes (1996). Interactions of CO2 enrichment and temperature on carbohydrate accumulation and partitioning in rice. Environ Exp Bot 36: 111-24.

Rudorff, B.F.T., C.L. Mulchi, E. Lee, R. Rowland, and R. Pausch (1996). Photosynthetic characteristics in wheat exposed to elevated O3 and CO2. Crop Sci 36: 1247-51.

Rufty, T.W., Jr., C.T. MacKown, and R.M. Volk (1989). Effects of altered carbohydrate availability on whole-plant assimilation of 15NO3-. Plant Physiol 89: 457-63.

Sage, R.F., T.D. Sharkey, and J.R. Seemann (1989). Acclimation of photosynthesis to elevated CO2 in five C3 species. Plant Physiol 89: 590-96.

Scheiner, S.M., and J.M. Rey-Benayas (1994). Global patterns of plant diversity. Evol Ecol 8: 331-47.

Samuelson, L.J., and J.R. Seiler (1992). Fraser fir seedling gas exchange and growth in response to elevated CO2. Environ Exp Bot 32: 351-56.

Sand-Jensen, K., M.F. Pedersen, and S. Laurentius (1992). Photosynthetic use of inorganic carbon among primary and secondary water plants in streams. Freshwater Biol 27: 283-93.

Scifres, C.J. (1980). Brush Management: Principles and Practices for Texas and the Southwest. College Station, TX: Texas A and M University Press.

Seemann, J.R., J.A. Berry, and J.S. Downton (1984). Photosynthetic response and adaptation to high temperature in desert plants. A comparison of gas exchange and fluorescence methods for studies of thermal tolerance. Plant Physiol 75: 364-68.

Shapiro, J. (1997). The role of carbon dioxide in the initiation and maintenance of blue-green dominance in lakes. Freshwater Biol 37: 307-23.

Sicher, R.C., and J.A. Bunce (1997). Relationship of photosynthetic acclimation to changes of Rubisco activity in field-grown winter wheat and barley during growth in elevated carbon dioxide. Photosyn Res 52: 27-38.

Sicher, R.C., and D.F. Kremer (1994). Responses of Nicotiana tabacum to CO2 enrichment at low-photon flux density. Physiol Plant 92: 383-88.

Simmons, G.L., and P.E. Pope (1987). Influence of soil compaction and vesicular-arbuscular mycorrhizae on root growth of yellow poplar and sweet gum seedlings. Can J For Res 17: 970-75.

--- (1988). Influence of soil water potential and mycorrhizal colonization on root growth of yellow-poplar and sweet gum seedlings grown in compacted soil. Can J For Res 18: 1392-96.

Sinclair, T.R., C.T. deWit (1975). Photosynthate and nitrogen requirements for seed productivity by various crops. Science 189: 565-67.

Smith, S.E., and D.J. Read (1996). Mycorrhizal symbiosis. London: Academic Press.

Sombroek, W.G. (1995). Aspects of soil organic matter and nutrient cycling in relation to climate change and agricultural sustainability. In International Symposium on Nuclear and Related Techniques in Soil-Plant Studies on Sustainable Agriculture and Environmental Preservation, Nuclear Techniques in Soil-Plant Studies for Sustainable Agriculture and Environmental Preservation (Vienna, AT: International Atomic Energy Agency): 15-26.

Spelsberg, G. (1987). Zum Problem der Beurteilung des Zuwachses in geschadigten Bestanden. Allg Forst Jagdztg 158: 205-10.

Spieker, M. (1990). Growth variation and environmental stresses: long-term observations on permanent research plots in southwestern Germany. Water Air Soil Poll 54: 247-56.

Stitt, M. (1991). Rising CO2 levels and their potential significance for carbon flow in photosynthetic cells. Plant Cell Environ 14: 741-62.

Strain, B.R., and J.D. Cure (1994). Direct effects of atmospheric CO2 enrichment on plants and ecosystems: an updated bibliographic data base. Oak Ridge, TN: Oak Ridge National Laboratory.

Stuhlfauth, T., and H.P. Fock (1990). Effect of whole season CO2 enrichment on the cultivation of a medicinal plant, Digitalis lanata. J Agron Crop Sci 164: 168-73.

Stulen, I., and J. den Hertog (1993). Root growth and functioning under atmospheric CO2 enrichment. Vegetatio 104/105: 99-115.

Svedang, M.U. (1992). Carbon dioxide as a factor regulating the growth dynamics of Juncus bulbosus. Aquatic Bot 42: 231-40.

Taiz, L.,and E. Zeiger (1991). Plant Physiology. Redwood City, CA: Benjamin-Cummings.

Teskey, R.O. (1995). A field study of the effects of elevated CO2 on carbon assimilation, stomatal conductance and leaf and branch growth of Pinus taeda trees. Plant Cell Environ 18: 565-73.

--- (1997). Combined effects of elevated CO2 and air temperature on carbon assimilation of Pinus taeda trees. Plant Cell Environ 20: 373-80.

Thomas, R.B., and B.R. Strain (1991). Root restriction as a factor in photosynthetic acclimation of cotton seedlings grown in elevated carbon dioxide. Plant Physiol 96: 627-34.

Thornley, J.H.M., and M.G.R. Cannell (1996). Temperate forest responses to carbon dioxide, temperature and nitrogen: a model analysis. Plant Cell Environ 19: 1331-48.

Tingey, D.T., M.G. Johnson, D.L. Phillips, D.W. Johnson, and J.T. Ball (1996). Effects of elevated CO2 and nitrogen on the synchrony of shoot and root growth in ponderosa pine. Tree Physiol 16: 905-14.

Tinker, P.B. (1984). The role of microorganisms in mediating and facilitating the uptake of plant nutrients from the soil. Plant Soil 76: 77-91.

Tissue, D.T., and W.C. Oechel (1987). Response of Eriophorum vaginatum to elevated CO2 and temperature in the Alaskan tussock tundra. Ecology 68: 401-10.

Titus, J.E. (1992). Submersed macrophyte growth at low pH. II. CO2 sediment interactions. Oecologia 92: 391-98.

Titus, J.E., R.S. Feldman, and D. Grise (1990). Submersed macrophyte growth at low pH. I. CO2 enrichment effects with fertile sediment. Oecologia 84: 307-313

Umali-Garcia, M., D.H. Hubbel, M.H. Gaskin, F.B. Dazzo (1980). Association of Azospirillum with grass roots. Appl Environ Microbiol 39: 219-26.

Van Oosten, J.-J., and R.T. Besford (1996). Acclimation of photosynthesis to elevated CO2 through feedback regulation of gene expression: climate of opinion. Photosyn Res 48: 353-65.

Vitousek, P.M., H.A. Mooney, J. Lubchenco, and J.M. Melillo (1997). Human domination of Earth's ecosystems. Science 277: 494-99.

Vogel, C.S., and P.S. Curtis (1995). Leaf gas exchange and nitrogen dynamics of N2-fixing, field-grown Alnus glutinosa under elevated atmospheric CO2. Global Change Biol 1: 55-61.

Volin, J.C., P.B. Reich (1996). Interaction of elevated CO2 and O3 on growth, photosynthesis and respiration of three perennial species grown in low and high nitrogen. Physiol Plant 97: 674-84.

Vu, J.C.V., L.H. Allen Jr., K.J. Boote, and G. Bowes (1997). Effects of elevated CO2 and temperature on photosynthesis and Rubisco in rice and soybean. Plant Cell Environ 20: 68-76.

Wang, K.-Y. (1996a). Apparent quantum yield in Scots pine after four years of exposure to elevated temperature and CO2. Photosynthetica 32: 339-53.

--- (1996b). Canopy CO2 exchange of Scots pine and its seasonal variation after four-year exposure to elevated CO2 and temperature. Agric For Meteorol 82: 1-27.

Wang K.-Y., and S. Kellomaki (1997). Effects of elevated CO2 and soil-nitrogen supply on chlorophyll fluorescence and gas exchange in Scots pine, based on a branch-in-bag experiment. New Phytol 136: 277-86.

Wang, K.-Y., S. Kellomaki, and K. Laitinen (1995). Effects of needle age, long-term temperature and CO2 treatments on the photosynthesis of Scots pine. Tree Physiol 15: 211-18.

Weaver, P.L., and P.G. Murphy (1990). Forest structure and productivity in Puerto Rico's Luquillo Mountains. Biotropica 22: 69--82.

Webber, A.N., G.-Y. Nie, S.P. Long (1994). Acclimation of photosynthetic proteins to rising atmospheric CO2. Photosyn Res 39: 413-25.

Weidenbach, P. (1992). Waldbauliche ziele und ergebnisse. Allg Forstzeitschr 13: 711-17.

West, D.C. (1988). Detection of forest response to increased atmospheric carbon dioxide. In F.A. Koomanoff (ed), Carbon Dioxide and Climate: Summaries of Research in FY 1988 (Wasington, DC: US Department of Energy): 57.

Wittwer SH (1995). Food, Climate, and Carbon Dioxide: The Global Environment and World Food Production. Boca Raton, FL: CRC Press/Lewis Publishers.

--- (1997). The global environment: it's good for food production. In P.J. Michaels (ed), State of the Climate Report: Essays on Global Climate Change (New Hope, VA: New Hope Environmental Services): 8-13.

Wood, C.W., H.A. Torbert, H.H. Rogers, G.B. Runion, and S.A. Prior (1994). Free-air CO2 enrichment effects on soil carbon and nitrogen. Agric For Meteorol 70: 103-16.

Woodrow, I.E. (1994). Optimal acclimation of the C3 photosynthetic system under enhanced CO2. Photosyn Res 39: 401-12.

Woodwell, G.M. (1989). The warming of the industrialized middle latitudes 1985-2050: causes and consequences. Climatic Change 15: 31-50.

Wullschleger, S.D., R.J. Norby, and C.A. Gunderson (1997). Forest trees and their response to atmospheric CO2 enrichment: a compilation of results. In L.H. Allen Jr., M.B. Kirkham, D.M. Olszyk, and C.E. Whitman (eds)., Advances in Carbon Dioxide Effects Research (Madiosn, WI: American Society of Agronomy): 79-100.

Wullschleger, S.D., R.J. Norby, and D.L. Hendrix (1992). Carbon exchange rates, chlorophyll content, and carbohydrate status of two forest tree species exposed to carbon dioxide enrichment. Tree Physiol 10: 21-31.

Wullschleger, S.D., W.M. Post, and A.W. King (1995). On the potential for a CO2 fertilization effect in forests: estimates of the biotic growth factor based on 58 controlled-exposure studies. In G.M. Woodwel, and F.T. Mackenzie (eds), Biotic Feedbacks in the Global Climatic System (Oxford: Oxford University Press): 85-107.

Zak, D.R., K.S. Pregitzer, P.S. Curtis, J.A. Teeri, R. Fogel, D.L. Randlett (1993). Elevated atmospheric CO2 and feedback between carbon and nitrogen cycles. Plant Soil 151: 105-17.

Ziska, L.H., B.G. Drake, and S. Chamberlain (1990). Long-term photosynthetic response in single leaves of a C3 and C4 salt marsh species grown at elevated atmospheric CO2 in situ. Oecologia 83: 469-72.

Ziska, L.H., R.C. Sicher, and D.F. Kremer (1995). Reversibility of photosynthetic acclimation of swiss chard and sugarbeet grown at elevated concentrations of CO2. Physiol Plant 95: 355-64.

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