© 2002 by The Society for Integrative and Comparative Biology
Atmospheric CO2 as a Global Change Driver Influencing Plant-Animal Interactions1
1 Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, Utah 84112-0840
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Plants respond to changes in atmospheric carbon dioxide. To herbivores, the decreased leaf protein contents and increased C/N ratios common to all leaves under elevated atmospheric carbon dioxide imply a reduction in food quality. In addition to these fine-scale adjustments, the abundance of C3 and C4 plants (particularly grasses) are affected by atmospheric carbon dioxide. C4 grasses currently predominate over C3 grasses in warmer climates and their distributions expand as atmospheric carbon dioxide levels decreased during glacial periods. C4 grasses are a less nutritious food resource than C3 grasses both in terms of reduced protein content and increased C/N ratios. There is an indication that as C4-dominated ecosystems expanded 6–8 Ma b.p., there were significant species-level changes in mammalian grazers. Today there is evidence that mammalian herbivores differ in their preference for C3 versus C4 food resources, although the factors contributing to these patterns are not clear. Elevated carbon dioxide levels will likely alter food quality to grazers both in terms of fine-scale (protein content, C/N ratio) and coarse-scale (C3 versus C4) changes.
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INTRODUCTION |
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Atmospheric gas composition plays an important role in determining many aspects of animal and plant metabolism (Körner, 2000
). Do changes in atmospheric composition, particularly of CO2 and O2, affect plants in fundamentally different ways than they do animals? On a short-term basis, the absolute concentrations of these two gases have immediate impacts on gas exchange rates of both animal and plants with their surrounding environment. For example, the concentrations of CO2 and O2 will influence the degree of O2 saturation of hemoglobin in animals and the extent of photorespiration in plants. While these responses might appear to have little in common, there is a common biochemical driver for the metabolic shifts: changes in the ratio of atmospheric CO2/O2. Such changes in atmospheric gas composition have occurred since the dawn of biological life several billion years ago and form the basis of different metabolic adaptations in both plants and animals. Changes in atmospheric gas composition can also influence plant-animal interactions in fundamentally different ways. Over a longer time scale of weeks, changes in the ratio of CO2/O2 in the atmosphere affects plant metabolism in ways that ultimately influence the quality of leaves as a food resource for animals. In this synthesis, we focus on how historical and current global changes in atmospheric CO2 have driven changes in plant metabolism at both a fine scale through adjustments in the relative composition of leaf-level biochemical components and at a coarse scale through shifts in the dominant photosynthetic pathway prevalent in a habitat. Both fine and coarse scale changes in leaf metabolism have direct and significant impacts on the quality of leaves as a food resource, thereby impacting animal performance in response to global atmospheric change.
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ATMOSPHERIC CO2 |
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Over the past 200 million years, the atmospheric CO2 concentrations have fluctuated, whereas on a relative basis the concentrations of atmospheric O2 are thought to have exhibited limited changes (Berner, 1991
, 1997; Petit et al., 1999; Ekart and Cerling, 1999). We can divide the recent history of atmospheric CO2 concentration into the distinct periods: 0.5–200 Ma before present, 0–420,000 yr before present, and since 1958 when high-precision and long-term CO2 records were first continuously collected (Fig. 1). Our understanding of long-term atmospheric CO2 is based on geochemical proxies, but there is reasonable agreement of a long-term decline in atmospheric CO2 from 
2,000+ ppm CO2 in the Cretaceous (about 75 million years ago) to much lower values before the Industrial Revolution began three centuries ago (Berner, 1997; Ekart and Cerling, 1999). At the moment, the fine scale estimates of atmospheric CO2 over the past 1–30 Ma are a subject of intense interest with various proxies being considered to estimate CO2 fluctuations over this period. Pagani et al. (1999a, b) used 
13C values of alkenones and carbonates in marine sediments to estimate atmospheric CO2 for the last 25 million years. Their results suggest that atmospheric CO2 had remained low (200–400 ppm) during this entire period, implying that the predicted CO2 threshold for C4 expansion may not have occurred. Instead Pagani and colleagues suggest that C4 expansion was triggered by global aridity. Quite independently, Pearson and Palmer (2000) used marine boron-isotope proxies to estimate that atmospheric CO2 levels had remained low (at or near today's levels of 370 ppm) for the past 60 Ma. However, the recent study by Lemarchand et al. (2000) revealed that oceanic boron isotope budgets are largely unconstrained and greatly influenced by shifts in the terrestrial inputs. Thus, one might only be able to conclude from boron isotope studies that atmospheric CO2 values (0–0.5 Ma b.p.) were 200–300 ppm. As will become evident shortly, knowledge of the high-resolution history of atmospheric CO2 is important for understanding the biological mechanisms responsible for shifts in photosynthetic pathway that ultimately impact animal diets.
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As a result of the Vostok ice-core studies (Fig. 1), we now know that atmospheric CO2 values shifted between 180 and 280 ppm as the Earth oscillated between glacial and interglacial periods over the past 420,000 yr (Petit et al., 1999
). What constrained the global atmospheric CO2 concentrations at these particular end points is not clear, but what is clear is both photosynthesis and the nutritional quality of leaves are particularly sensitive to changes in atmospheric CO2 over this range (Sage and Monson, 1999). Thus, as the Earth cycled between glacial and interglacial periods, both terrestrial productivity and the quality of food available to herbivores are likely to have undergone significant swings.
Global atmospheric changes are occurring today—only this time humans are the drivers of these changes and not glacial-interglacial cycles. Today we have entered a new period in the Earth's history where humans are having a significant impact on atmospheric CO2 values (Fig. 1). Beginning with the use of fossil fuels in the Industrial Revolution and the acceleration since the 1950s, humans now have a dominant and ever increasing impact on the Earth's atmosphere. Atmospheric CO2 levels today exceed values recorded in the Vostok core by more than 30%. We are now entering a selective regime where CO2 in the atmosphere exceeds the natural range under which most extant plant and animal species are thought to have evolved. This global change in the atmosphere does have direct and indirect impacts on species at the metabolic and evolutionary levels as well as on the functioning of ecosystems through impacts on both productivity and carbon cycling (Mooney et al., 1999). We next examine how global atmospheric CO2 changes impact both plant metabolism and in turn impact the diet quality available for animals.
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ATMOSPHERIC CO2 IMPACTS DIET QUALITY |
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Food quality is hard to precisely define, yet there is no doubt that four parameters influencing palatability of foods include leaf protein content, soluble carbohydrate content, fiber content, and the abundance of different secondary compounds. Changes in atmospheric CO2 will impact food quality for herbivores at both fine and coarse scales.
At a fine scale, leaves acclimate to changes in atmospheric CO2 through adjustments in leaf protein levels, carbohydrate content, and leaf thickness (Overdieck et al., 1988; Curtis and Wang, 1998; Cowling and Sage, 1998; Diaz et al., 1998; Wand et al., 1999). Overall, these changes result in adjustments in the C/N ratios of leaves, which in turn should impact food quality as perceived by herbivores. In response to increasing atmospheric CO2, protein levels decrease in leaves of all species (Fig. 2). Comparisons are typically made with leaves of plants grown at 2x current ambient CO2 (650–700 ppm), which are the anticipated levels within a century from now. The down regulation of photosynthesis results in 10–20% lower leaf nitrogen levels, since much of the soluble leaf protein is associated with RuBP carboxylase (Rubisco) (Sage, 1994; Cowling and Sage, 1998; Wand et al., 1999). Even though photosynthesis is down regulated, leaves tend to accumulate greater sugar and starch levels resulting in non-structural carbohydrate levels that are 10–40% higher than levels observed in plants grown under today's CO2 conditions. Overall, the C/N ratios of leaves increase by 20–30% under 2x elevated CO2 conditions; these responses occur in both C3 and C4 photosynthetic pathway plants (Fig. 2).
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Both mammalian and insect herbivores respond to leaves grown under elevated CO2 with responses resulting in slower growth rates. In insects, these responses range from modified ingestion rates to longer maturation times (Arnone et al., 1995
; Agrell et al., 2000; Körner, 2000). In cattle, there is some evidence for possible reduced growth rates of steers, particularly in spring when leaves have their highest protein contents under today's CO2 conditions (Owensby et al., 1996). Most of these responses fit into the general category of reduced digestibility and can be directly related to leaf C/N ratios. At the plant species level, plant secondary compound production will impact herbivores in species-specific ways. These secondary compounds tend to increase by as much as two-fold in defensive compounds produced via the shikimic acid pathway and little if at all in secondary compounds derived via the malvionic acid pathway (Roth et al., 1998; McDonald et al., 1999; Agrell et al., 2000).
Fewer studies are available for understanding how plants respond to atmospheric CO2 levels that existed during pre-Industrial periods and during glacial periods (Overdieck et al., 1988; Polley et al., 1992, 1993; Ward et al., 1999). The pattern is opposite to that observed for leaves grown under high CO2 (Fig. 2). In subambient CO2, leaves have slower growth rates and as a result nonstructural carbohydrate levels are reduced. Leaf nitrogen content tends to be higher. We are aware of no studies that have examined animal feeding patterns and preferences for leaves grown under subambient CO2 levels.
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C4 PLANTS AS A FOOD RESOURCE |
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It is important to distinguish fine-scale acclimation changes in food quality from the relatively large coarse-scale differences in food quality associated with leaves having C3 versus C4 photosynthesis. Historically, feeding trials and food preference studies have tended not to distinguish between leaves of plants having one photosynthetic pathway versus the other. Many feeding studies do distinguish between forbs and grasses as substrate; in most cases these studies involve C3 x C3 comparisons and in only a few are there C3 x C4 comparisons. Yet as early as a quarter century ago, Caswell et al. (1973)
hypothesized that C4 plants were nutritionally inferior to C3 plants. They hypothesized that animals in general avoided C4 plants, but today we recognize that animals often exhibit distinct preferences for either C3 or C4 species (Ehleringer and Monson, 1993; Heckathorn et al., 1999).
Although C4 photosynthesis occurs in less than 2% of higher plant species, it accounts for 25% of today's primary productivity (Ehleringer et al., 1997; Collatz et al., 1998; Sage and Monson, 1999). Approximately half of the 10,000 grass and sedge species have C4 photosynthesis, but fewer than 2,000 of the dicotyledonous species exhibit C4 photosynthesis. Given their disproportionate influence on global productivity, C4 plants have attracted much attention by the ecophysiological and ecosystem communities (Sage and Monson, 1999). Yet our understanding of animal preferences for C3 versus C4 plants is still limited (Heckathorn et al., 1999). Carbon isotope ratio (13C) analyses of modern mammalian herbivore teeth suggest that mammals exhibit a distinct preference for either C3 or C4 taxa, with limited number of species being mixed feeders (Fig. 3). McNaughton and Georgiadis (1986) and references within Heckethorn et al. (1999) suggest that mammals exhibit limited preference for C3 versus C4, but that the primary differences in the African savanna are tree/shrub (C3) versus grass (C4) feeding patterns. In contrast, feeding trials repeatedly show that the digestibility of C4 plants by mammalian grazers is lower than for C3 plants (Aiken et al., 1983; Wilson and Hattersley, 1983, 1989; Wilson, 1991; Wilson et al., 1991). The basis for dietary preference of C3/C4 grasses by mammalian grazers is not understood at the moment. Nevertheless, the available evidence suggests that C3/C4 dietary differences do play a role in diet selection. Since the earliest carbon-isotope insect field studies, a C3/C4 dietary preference has been evident (Boutton et al., 1978; Fry et al., 1978; Heidorn and Joern, 1984). Caswell and Reed (1976) showed that when grasshoppers normally feeding on C3 grasses were fed a C4 grass, much of the leaf tissue passed through the crop undigested.
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The dietary quality of C3 and C4 grasses is different. C4 grasses maintain lower protein contents than do C3 grasses (120–180 versus 200–260 mol N m–2) (Ehleringer and Monson, 1993
). In grasses, fiber content is higher than that of dicotyledonous leaves, especially since fibers are often associated with vascular tissues and grasses tend to have a more prominent and common vascular system (when compared to dicotyledonous leaves) (Sage and Monson, 1999). In C4 grasses, the interveinal distances are shorter than those of C3 grasses (Kawamitsu et al., 1985; Dengler et al., 1994; Dengler and Nelson, 1999). As a result the C/N ratio is much higher in C4 grasses than in C3 grasses (Fig. 4). The C/N ratio impacts both grazing efficiency and diet selection, suggesting that C4 plants should be a less preferred food resource.
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ATMOSPHERIC CO2 AS A DRIVER OF C3/C4 DISTRIBUTIONS |
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The initial CO2 fixation reaction in photosynthesis involves the carboxylation of ribulose bisphosphate by the enzyme Rubisco to form 2 molecules of phosphoglyceric acid, a 3-carbon molecule and hence the name C3 photosynthesis. Under reduced CO2 partial pressures, this enzyme also exhibits an oxygenase activity, such that at today's partial pressures, approximately 1 out of every 5 Rubisco cycles results in an oxygenase activity and not a carboxylation reaction (Kanai and Edwards, 1999
). This oxygenase activity results in the evolution of CO2 (photorespiration) and reduces the net carbon fixation into sugars by approximately 30% (Ehleringer, 1978; Ehleringer and Björkman, 1977; Sage and Monson, 1999; Sage and Pearcy, 2000). The rate at which the carboxylase versus oxygenase activity is expressed is a direct function of the atmospheric CO2/O2 ratio and so changes in global atmospheric composition will have a significant impact on photorespiratory rates.
One evolutionary solution to increased photorespiration under reduced atmospheric CO2 is C4 photosynthesis, where the normal C3 cycle is restricted to the interior of the leaf and external to this the mesophyll cells catalyze the initial reaction: CO2 combines with phosphoenolpyruvate to form a C4-acid (Kanai and Edwards, 1999; Sage and Pearcy, 2000). This pathway appears in approximately 30 advanced Angiosperm families (see compilations in Ehleringer et al., 1997; Sage and Monson, 1999) and is thought to have evolved independently at least 18 different times (Kellogg, 1999). C4 photosynthesis is by far most common in grasses and sedges (6,000+ species) and less common in dicots (1,500+ species).
The modern distribution of C4 grasses and sedges is determined primarily by temperature during the growing season, assuming that soil moisture is available (Teeri and Stowe, 1976; Collatz et al., 1998). Grasses make up important components of ecosystems where rainfall is approximately equal to potential evapotranspiration; geographically this includes the tropical savannas, temperate to boreal steppes, and tropic to temperate semi-arid grasslands and deserts.
Cerling et al. (1997) and Ehleringer et al. (1997) modeled the fitness relationships between C3 and C4 taxa. Given similar canopies, differences in the light-use efficiencies of the two pathways result in distinct climate spaces favoring one photosynthetic pathway over the other (Fig. 5). At any given point in time, the atmospheric CO2 value is constant, resulting in C3 plants being more favored in cooler climates and C4 plants in warmer climates, As the global atmospheric CO2 values decreased, this model predicts that C4 taxa should have first dominated in the warmest habitats and progressively expand poleward as atmospheric levels decreased (such as during glacial periods). Today's C4 grass and sedge distributions are consistent with this model.
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The quantum yield model of Figure 5 predicts that, at some time in the Earth's history, atmospheric CO2 levels became low enough to cross a threshold which favored C4 grasses over C3 grasses. Cerling et al. (1997)
reported that at 6–8 Ma b.p. there was an abrupt emergence of C4 grasslands on a global scale. Using the 13C values of enamel in fossil teeth, there is a clear indication of the simultaneous expansion of C4 grasslands (Fig. 6). In some locations, such as Pakistan, C4 grasslands replaced C3 grasslands. In other locations, such as North America, C3 and C4 taxa both persisted, but likely temporally or spatially separated along environmental gradients.
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The expansion of C4 photosynthesis 6–8 Ma b.p. coincides with changes in the abundances of mammalian grazers (Fig. 7). Cerling et al. (1998)
measured the turnover of mammalian fauna through estimates of the number of new taxa added to a region and the disappearance of taxa from a region over time. They showed that the period 6–8 Ma b.p. was associated with an increased turnover rate among grazing mammals. The exact causes of the emergence and loss of taxa are not established, but it is an unusual coincidence that it occurred during the same period as the global expansion of C4 ecosystems. Diet is possibly an important consideration here. However, given the apparent selectivity of mammals for C3 versus C4 taxa (Fig. 3), it is possible that diet and mammalian turnover are related in more than a coincidental manner.
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The quantum yield model of Figure 5 predicts a C4 expansion during glacial periods when atmospheric CO2 was low (
180 ppm) and a C4 contraction during interglacial periods and contraction as atmospheric CO2 increased to 280 ppm. There is strong global evidence of C4 expansion during glacial periods from a variety of sources. These data occur as 13C data from bogs, lake sediments, carbonates, and fossil bone materials from equatorial and temperate regions (Street-Perrott et al., 1998; Huang et al., 1999). The bog and lake sediment data are a largely continuous record of plant materials flowing into these basins, spanning 0–30 ka b.p. for lakes in Mexico and central Africa to 0–400 ka b.p. for the FUNZA II core in Colombia. Each of the cores indicate a loss of C4 species at the end of the Last Glacial Maximum and a reversion to C3-dominated ecosystems. The soil carbonate data are from caliche in the arid Southwest of North America and indicate ecosystems dominated by C4 vegetation in areas now dominated by C3 vegetation. Based on tooth enamel studies, mammoths, camels, and equids, that lived during the last glacial in western North America contained a significant C4 fraction in their diets (Connin et al., 1998).
The emergence of generalized patterns and the mechanistic basis for why animals might prefer C3 versus C4 diets remain to be clarified. Although there is evidence that digestion efficiencies of animals differ when fed C3 versus C4 grasses (Wilson, 1991), the extent to which differences in digestion impact animal efficiency are speculative at the moment. Yet there is reason to believe that dietary efficiency and fitness should be correlated with each other.
It is anticipated that atmospheric CO2 levels will be double the current values by the end of this century. Until mankind's thirst for fossil fuels is quenched, it is likely that atmospheric CO2 will continue to rise beyond levels experienced in the recent history of this planet. The quantum yield model predicts that as CO2 levels rise, the atmosphere concentrations will once again cross the CO2-threshold where C4 plants do not have a competitive advantage over C3 plants from the standpoint of reduced photorespiration and enhanced light-use efficiency. Will C4 plants disappear in the future? That answer is unclear, because other aspects of global change are occurring, which also tend to favor C4 taxa. These additional global changes include forest to grassland conversions (particularly in the tropics), biological invasions (particularly weedy species), and the fact that many of today's most prominent crops are C4 plants (e.g., corn and sorghum). Regardless of whether or not C4 plants are as common among subtropical and tropical ecosystems, changes in atmospheric CO2 will have continued impacts on the quality of forage available for herbivores.
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ACKNOWLEDGMENTS |
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The materials presented in this manuscript were supported by a grant from the Packard Foundation and participation in the symposium by NSF grant IBN-0097876.
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FOOTNOTES |
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1 From the symposium Plant/Animal Physiology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 E-mail: ehleringer{at}biology.utah.edu
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References |
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