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Keywords:

  • atmospheric change;
  • crop yield;
  • elevated [CO2];
  • FACE (free air CO2 enrichment);
  • leaf area;
  • photosynthesis;
  • Rubisco

Abstract

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

Contents

  •  Summary 1

  • I. 
    What is FACE? 2
  • II. 
    Materials and methods 2
  • III. 
    Photosynthetic carbon uptake 3
  • IV. 
    Acclimation of photosynthesis 6
  • V. 
    Growth, above-ground production and yield 8
  • VI. 
    So, what have we learned? 10
  •  Acknowledgements 11

  •  References 11

  • Appendix 1. References included in the database for meta-analyses  14

  •  Appendix 2. Results of the meta-analysis of FACE effects 18

Summary

Free-air CO2 enrichment (FACE) experiments allow study of the effects of elevated [CO2] on plants and ecosystems grown under natural conditions without enclosure. Data from 120 primary, peer-reviewed articles describing physiology and production in the 12 large-scale FACE experiments (475–600 ppm) were collected and summarized using meta-analytic techniques. The results confirm some results from previous chamber experiments: light-saturated carbon uptake, diurnal C assimilation, growth and above-ground production increased, while specific leaf area and stomatal conductance decreased in elevated [CO2]. There were differences in FACE. Trees were more responsive than herbaceous species to elevated [CO2]. Grain crop yields increased far less than anticipated from prior enclosure studies. The broad direction of change in photosynthesis and production in elevated [CO2] may be similar in FACE and enclosure studies, but there are major quantitative differences: trees were more responsive than other functional types; C4 species showed little response; and the reduction in plant nitrogen was small and largely accounted for by decreased Rubisco. The results from this review may provide the most plausible estimates of how plants in their native environments and field-grown crops will respond to rising atmospheric [CO2]; but even with FACE there are limitations, which are also discussed.


I. What is FACE?

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

The rise in atmospheric carbon dioxide concentration [CO2], is one of the best documented global atmospheric changes of the past half century (Prentice, 2001). Enormous research efforts have been undertaken to understand how plants and ecosystems, both natural and managed, will respond to rising [CO2]. The primary effects on plants of rising [CO2] have been well documented and include reduction in stomatal conductance and transpiration, improved water-use efficiency, higher rates of photosynthesis, and increased light-use efficiency (Drake et al., 1997). The majority of these conclusions have come from studies of individual species grown in controlled environments or enclosures (for reviews see Kimball, 1983; Ceulemans & Mousseau, 1994; Gunderson & Wullschleger, 1994; Amthor, 1995; Curtis, 1996; Drake et al., 1997; Curtis & Wang, 1998; Saxe et al., 1998; Norby et al., 1999; Wand et al., 1999). While the conclusions from these experiments form the basis for our knowledge of plant physiological responses to elevated [CO2], there are serious potential limitations to using enclosure systems when studying the effects of elevated [CO2] on plants. Enclosures may amplify downregulation of photosynthesis and production (Morgan et al., 2001), and may through environmental modification produce a ‘chamber effect’ that exceeds the effect of elevating [CO2]. Chambers also are limited in size and may have limited capacity to allow investigators to follow trees and crops to maturity within a valid experimental design (McLeod & Long, 1999). Further, growing plants in pots restricts the rooting volume and suppresses plant responses to elevated [CO2] (Arp, 1991).

Large-scale free-air CO2 enrichment (FACE) experiments allow the exposure of plants to elevated [CO2] under natural and fully open-air conditions. FACE technology uses no confinement structures, rather an array of vertical or horizontal vent pipes to release jets of CO2-enriched air or pure CO2 gas at the periphery of vegetation plots. FACE relies on natural wind and diffusion to disperse the CO2 across the experimental area. The first FACE systems utilized blowers or fans to inject CO2-enriched air into the treatment area (Hendrey et al., 1993; Lewin et al., 1994). More recent field studies have employed a FACE technique in which pure CO2 gas is released as high-velocity jets from emission tubes (through numerous small perforations) positioned horizontally at the periphery of a FACE octagon (Miglietta et al., 2001; Okada et al., 2001). FACE design allows good temporal and spatial control of CO2 concentrations throughout crop canopies and also relatively young homogeneous forest plantations (Hendrey et al., 1999).

This review focuses on the large-scale FACE facilities (8–30 m diameter) that have been established on forest, grassland, desert and agriculture lands (Table 1). These FACE experiments expose vegetation to elevated [CO2] of 475–600 ppm, encompass a large number of species and functional groups as well as soil fertilization and stress treatments, and have reduced edge effects compared with small-scale (1–2 m diameter) FACE rings. The results of two multisite, mini-FACE experiments, Bog Ecosystem Research Initiative (BERI) and Managing European Grasslands as a Sustainable Resource in a Changing climate (MEGARICH), were recently reviewed along with some of the large-scale FACE studies (Nowak et al., 2004). In this review the results of large-scale FACE experiments were assessed quantitatively using meta-analytic statistical methods. The second purpose of this review was to compare and contrast the results of chamber-based studies with those of FACE experiments. Only side-by-side tests of open-top chambers and FACE technology, on the same soil with the same level of CO2 fumigation, will allow a direct comparison of [CO2] responses in FACE and in open-top chambers. In the absence of such experiments, some guide to differences may be made by quantitatively summarizing results obtained from the two techniques using a meta-analytic approach. This has been done here. It is also evident from Table 1 that FACE experiments have focused on temperate ecosystems, while tropical, boreal and arctic systems have been largely ignored. Any serious commitment to discovering the response of the terrestrial biosphere to atmospheric change will critically require inclusion of these key biomes.

Table 1.  Large-scale free-air CO2 enrichment (FACE) facilities used in this review
SiteLocationElevated [CO2]Site description referenceEcosystemFirst year of exposure (ppm)
Aspen FACE FACTS 2Rhinelander, WI, USA 45°36′-N, 89°42′-WAmbient + 200Dickson et al. (2000)Aspen forest1998
BioCON Cedar CreekCedar Creek, MN, USA 45°24′-N, 93°12′-W550Reich et al. (2001)Natural prairie grassland1998
ETH-Z FACE Swiss FACEEschikon, Switzerland 47°27′-N, 8°41′-E600Zanetti et al. (1996)Managed grassland1993
FACTS 1 Duke ForestOrange County, NC, USA 35°58′-N, 70°5′-WAmbient + 200Hendrey et al. (1999)Loblolly pine forest1996
Maricopa FACEMaricopa, AZ, USA 33°4′-N, 111°59′-W550* Ambient + 200Lewin et al. (1994)Agronomic C3 and C4 crops1989
Nevada DesertMojave Desert, NV, USA 36°49′-N, 115°55′-W550Jordan et al. (1999)Desert ecosystem1997
Oak RidgeRoane County, TN, USA 35°54′-N, 84°20′-WAmbient + 200Norby et al. (2001)Sweetgum plantation1998
Pasture FACEBulls, New Zealand 40°14′-S, 175°16′-E475Edwards et al. (2001)Managed pasture1997
POPFACEViterbo, Italy 42°37′-N, 11°80′-EAmbient + 200Miglietta et al. (2001)Poplar plantation1999
Rapolano Mid FACEChianti Region, Italy 43°25′-N, 11°35′-E560–600Miglietta et al. (1997)Vitis vinifera Solanum tuberosum1995
Rice FACEShizukuishi town, Japan 39°38′-N, 140°57′-EAmbient + 200Okada et al. (2001)Oryza sativa1998
SoyFACEChampaign, IL, USA 40°02′-N, 88°14′-W550 Glycine max Zea mays2000

II. Materials and methods

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

Literature searches of primary FACE research in published peer-reviewed journals were conducted with the Current Contents citation index and the ISI Web of Science citation database. Data from 124 manuscripts that analyzed more than 40 species from 12 FACE sites were extracted for the analysis of gas exchange, leaf chemistry, leaf area and yield variables (Appendix 1). Response means of variables, standard deviations, and sample sizes from elevated and ambient [CO2] treatments were either taken from tables, digitized from figures using digitizing software (Morgan et al., 2003), or obtained directly from the authors of the primary studies.

Meta-analytic techniques have been developed for quantitative integration of research results from independent experiments (Hedges & Olkin, 1985), and have been widely adapted to summarize the effects of elevated [CO2] on vegetation (Curtis, 1996; Curtis & Wang, 1998; Medlyn et al., 1999, 2001; Kerstiens, 2001; Ainsworth et al., 2002, 2003). For this review, responses of different species, cultivars and stress treatments, and from different years of the FACE experiments, were considered to be independent and suited to meta-analytic analysis. Thus one FACE experiment examining a number of species in a multifactorial design could contribute multiple observations to a given response variable (e.g. Curtis & Wang, 1998; Ainsworth et al., 2003).

The natural log of the response ratio (r = response in elevated [CO2]/response in ambient [CO2]) was used as the metric for analyses (Hedges et al., 1999; Rosenberg et al., 2000), and is reported as the mean percentage change [(r – 1) × 100] at elevated [CO2]. The meta-analysis procedure followed the techniques described by Curtis & Wang (1998), using the statistical software metawin (Rosenberg et al., 2000). A mixed-model analysis was used, based on the assumption of random variation in effect sizes between FACE studies. A weighted parametric analysis was used, and each individual observation of response was weighted by the reciprocal of the mixed-model variance, which is the sum of the natural log of the response ratio and the pooled within-class variance (Hedges et al., 1999). If a 95% confidence interval did not overlap with zero, then a significant response to elevated [CO2] was considered.

Differences in the effect size of different categorical groups were tested according to the method of Curtis & Wang (1998). The approach taken was to partition total heterogeneity within and between levels of each categorical variable. For example, the photosynthetic type was either C3 or C4, and by dividing all species into those groups we could test whether there was significant between-group heterogeneity with respect to photosynthetic type. Partitioning of variance proceeded in two steps (Curtis & Wang, 1998). Between-group heterogeneity (QB) for each category was examined, then the data were subdivided according to levels of those categorical variables revealing significant between group heterogeneity. The between-group heterogeneity for CO2 effect size for each variable (Asat, crop yield, etc.) is shown in Table 2.

Table 2.  Between-group heterogeneity for CO2 effect size across categorical variables
VariablekPhotosynthesis type (C3 vs C4)Functional groupSiteStress
  • *

    P < 0.05;

  • **

    P < 0.01;

  • ***

    P < 0.001.

  • Light-saturated CO2 uptake (Asat), diurnal carbon assimilation (A′), apparent maximum quantum yield of CO2 uptake (AQY), stomatal conductance (gs), ratio of intercellular (ci) to atmospheric CO2 concentration (ca), instantaneous transpiration efficiency (ITE), maximum carboxylation rate (Vc,max), maximum rate of electron transport (Jmax), ratio of Vc,max : Jmax, Rubisco content in mass/unit area (Rubisco), N content on an area, mass and percentage basis, Narea, Nmass, N(%), respectively, chlorophyll content on both an area and mass basis (Chlarea, Chlmass), chlorophyll a : chlorophyll b (chl a : b), sugar content in mass/unit area (sugar), starch content in mass/unit area (starch), leaf-area index (LAI), specific leaf area (SLA), above-ground dry matter production (DMP). Blank spaces indicate that categorical analysis was not possible because only one category was represented. Blanks occur in the photosynthesis type column when only information for C3 species was available. Blanks in the functional group column occur when information for only one functional group was available, and in the stress column when no stress treatments were imposed. Each response was represented by k studies.

Asat32722.90***127.94***150.41**19.19**
A146 4.77* 24.09** 58.36*** 1.56
AQY 21   24.06*13.05
gs235 1.01 24.09** 41.51***25.77**
ci : ca 48  28.27** 24.79*** 8.26*
ITE 3518.87*** 26.50*** 23.07**19.51**
Vc,max228  15.28* 18.76*23.99***
Jmax168  36.49*** 57.03***12.66*
Vc,max/Jmax 97  13.79* 21.03 0.28
Rubisco 24   0.34  2.28 2.59
Narea124  24.21*** 25.17**14.68**
Nmass100  27.95*** 28.52***10.86*
N (%) 33   11.94*21.19**
Chlarea 40   0.085  0.11 0.345
Chlmass 32    2.93 
Chl a : b 20   1.76  1.89 0.66
Sugar 31   5.00  4.82 7.52
Starch 31  15.36** 15.72*13.25**
Plant height 59  15.24** 18.64* 0.42
Stem diameter 54   1.87 10.97* 5.54*
Leaf number 45   8.71 32.45* 2.63
LAI 54   5.32  5.24 1.67
SLA11410.26** 15.55* 18.10* 7.25
DMP17516.34** 65.26*** 12.71 4.13
Crop yield 28 9.65**   3.6117.21**

III. Photosynthetic carbon uptake

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

Elevated [CO2] increases photosynthesis by increasing the carboxylation rate of Rubisco and competitively inhibiting the oxygenation of Ribulose-1,5-bisphosphate (RubP) (Drake et al., 1997). Exposure to elevated [CO2] resulted in a 31% increase in the light-saturated leaf photosynthetic rate (Asat) and a 28% increase in the diurnal photosynthetic carbon assimilation (A′) when averaged across all FACE experiments and species (Fig. 1; Appendix 2). Apparent maximum quantum yield increased by 12%. Stomatal conductance (gs) was reduced by 20% with growth at elevated [CO2] when averaged for 40 species grown at all 12 FACE experiments (Fig. 1). Growth under stressful conditions (low N and drought) exacerbated the decrease in gs. There was no apparent change in the ratio of intercellular [CO2] : atmospheric [CO2] (ci : ca), and the instantaneous transpiration efficiency of plants grown under elevated [CO2] was stimulated by ≈ 50% (Fig. 1). A number of experimental variables significantly altered the response of photosynthetic carbon uptake to elevated [CO2], and are discussed further.

image

Figure 1. Mean response to elevated [CO2] (±95% CI) of light-saturated CO2 uptake (Asat), diurnal carbon assimilation (A′), apparent quantum yield of CO2 uptake (AQY), stomatal conductance (gs), ratio of intercellular (ci) to atmospheric CO2 concentration (ca), and instantaneous transpiration efficiency (ITE). Number of species, FACE experiments and individual observations for each response are given in Appendix 2.

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1. C3 vs C4 species

The number of C3 species investigated in large-scale FACE experiments is eight times greater than the number of C4 species. This is due in part to the assumption, based on photosynthetic theory, that C4 species would not benefit from increases in atmospheric [CO2] (Bowes, 1993). However, in a meta-analytic review of wild C3 and C4 grass (Poaceae) species, Wand et al. (1999) found similar increases in the assimilation response of C3 and C4 species (33 and 25% increases, respectively). Our analysis of C4 species was limited to only five species, but the results contrast very sharply with the analysis of Wand et al. (1999). Here, Asat was stimulated by elevated [CO2] in both C3 and C4 species, but the magnitude of the response was three times greater in C3 than C4 species (Fig. 2). Asat of three ‘wild’ C4 grasses grown at the BioCON experiment was not stimulated with growth at elevated [CO2], and Asat of C4 crops grown at the Maricopa and SoyFACE sites was increased by 20 and 15%, respectively. Photosynthetic stimulation is not necessarily expected in C4 species because of the CO2-concentrating mechanism in C4 leaves (Bowes, 1993; Ghannoum et al., 2000). There is variation in the CO2 saturation level of C4 leaves. While some species appear to be CO2 saturated at ambient [CO2], other C4 grasses are not necessarily saturated at that level (reviewed by Wand et al., 1999). Wand et al. (1999) suggest that this simple explanation may account for the variation in stimulation of photosynthesis in C4 species grown at elevated [CO2].

image

Figure 2. Comparative photosynthetic responses of C3 and C4 species to elevated [CO2] enrichment. ○, Results from this meta-analysis; ▴, comparative results from a prior meta-analysis of C3 and C4 wild grass (Poaceae) species (Wand et al., 1999). Number of species, FACE experiments and individual observations for each response in our meta-analysis are given in Appendix 2.

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Stomatal conductance (gs) decreased on average by 20% in elevated [CO2] and there was no difference between C3 and C4 species (Fig. 2). Wand et al. (1999) reported a similar magnitude of decrease in gs for both C3 and C4 grasses. The instantaneous transpiration efficiency (ITE, A/gs), a leaf-level measure of water-use efficiency, was significantly different between C3 and C4 species (Fig. 2; Appendix 2). C3 species grown under FACE had a 68% increase in ITE, while ITE was not increased in C4 species, based on six independent measurements of sorghum. However, individual studies reported that elevated [CO2] improved the water status and increased the water-use efficiency in sorghum in the Maricopa FACE experiment (Conley et al., 2001; Wall et al., 2001). The discrepancy between the Wand et al. (1999) report and this review illustrates one of the shortcomings of FACE to date. Only five C4 species have been investigated in large-scale FACE experiments, while Wand et al. (1999) reviewed 20 wild C4 species from 48 enclosure studies. Further FACE experiments on more C4 species are needed to resolve the discrepancy or confirm the differences between C4 responses to elevated [CO2] in chamber studies and FACE experiments.

2. C3 functional groups and FACE sites

There was a significant difference in the response of Asat to elevated [CO2] in different C3 functional groups (QB = 83.928, P < 0.001). Trees showed the greatest response to elevated [CO2], followed by fertilized C3 crops and C3 grasses (Fig. 3). Shrubs and legumes both showed a 21% increase in Asat with growth at elevated [CO2], and forbs showed approximately 15% increase in Asat (Fig. 3). The 47% increase in Asat for trees is significantly higher than the previously reported 31% increase for FACE-grown trees (Curtis & Wang, 1998), but is consistent with the 51% increase in Asat reported for European tree species grown under elevated [CO2] in field chambers (Medlyn et al., 1999; Fig. 3). Nowak et al. (2004) also reported that woody species showed a stronger enhancement in Asat relative to herbaceous species. This review includes values for trees grown under both elevated [CO2] and elevated [O3] at the Rhinelander FACE experiment. Ozone considerably increased the percentage response of Asat to elevated [CO2] (59% stimulation with growth under high [O3] and [CO2], relative to plants grown only in elevated [O3]; Appendix 2).

image

Figure 3. Comparative photosynthetic responses of different C3 functional groups to elevated [CO2]. Results from: ○, this meta-analysis; ▪, a meta-analysis of tree species (Curtis & Wang, 1998); ◆, a meta-analysis of European tree species (Medlyn et al., 2001); ▴, a meta-analysis of C3 grasses (Wand et al., 1999). Number of species, FACE experiments and individual observations for each response in our meta-analysis are given in Appendix 2.

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The same trends in functional groups were not observed when photosynthesis was measured and integrated over the diurnal period, although this is based on a much smaller number of studies. A′ was stimulated most in shrubs and grasses (Fig. 3). A′ was 29% higher in trees and ≈ 20% higher in legumes grown under elevated [CO2].

The experimental site also affected how a functional group responded to elevated [CO2] (Appendix 2). Photosynthetic stimulation of plants grown at the BioCON experiment was less than that of plants grown at the Swiss FACE and SoyFACE experiments. C3 grasses grown at the BioCON experiment showed a 16% increase in Asat, while Lolium perenne at the Swiss FACE experiment had a 41% increase in Asat (Appendix 2). The difference in response in the two systems was probably caused by nutrient status and reductions in leaf N content in species grown at the BioCON experiment (Nowak et al., 2004). The Swiss FACE experiment was a managed agricultural pasture (with 10–14 or 42–56 g N m−2 yr−1; Zanetti et al., 1996), and the BioCON experiment was a natural prairie grassland experiment with no nutrient input on some plots and 4 g N m−2 yr−1 on other plots (Reich et al., 2001). Even under low N-fertilization input typical of low-intensity grassland management, L. perenne showed an approximately 40% increase in Asat on average over the 10 yr experiment (Ainsworth et al., 2003). Legumes grown at the BioCON experiment did not show any stimulation in Asat with growth at elevated [CO2]. Asat of legumes grown at the Swiss FACE experiment and the SoyFACE experiment was stimulated by 37 and 22%, respectively.

The decrease in gs with elevated [CO2] was consistent with previously reported decreases in gs for European tree species (Medlyn et al., 2001). However, the decrease in gs varied with site (Table 2). Plants under FACE at the Eschikon experiment, which had the highest elevated [CO2] (600 ppm; Table 1), showed the greatest decrease in gs (≈ 33%; Appendix 2). Poplar species in the PopFACE experiment did not show any change in gs with growth at elevated [CO2] (Table 2; Appendix 2).

3. Temperature and stress

Stimulation of photosynthesis at elevated [CO2] is theoretically predicted to be greater at higher temperatures (Drake et al., 1997). When the FACE data were divided between experiments conducted below 25°C and those conducted above 25°C, this prediction was supported. At lower temperatures (< 25°C) Asat was increased by 19%, and at temperatures above 25°C Asat was increased by 30% when plants were grown under elevated [CO2] (QB = 5.37, P < 0.05; Fig. 4).

image

Figure 4. Comparative responses of light-saturated CO2 uptake (Asat) and stomatal conductance (gs) in different growth temperatures and stress treatments. Number of species, FACE experiments and individual observations for each response are given in Appendix 2.

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Ozone tended to enhance the response of Asat to elevated [CO2], and low N tended to reduce the response (Fig. 4). On average, plants grown without stress showed a 36% stimulation in Asat, trees in Rhinelander grown under high ozone showed a 59% stimulation, and plants grown under low-N treatment showed a 27.5% stimulation. Stress also significantly affected gs (Table 2). In general, decreases in gs with elevated [CO2] were exacerbated by low N and drought stress (Fig. 4).

IV. Acclimation of photosynthesis

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

To maintain a balance in N and other resources allocated to the reactions that control photosynthesis, species acclimate to growth in elevated [CO2] (Sage, 1990; Gunderson & Wullschleger, 1994; Drake et al., 1997). A reduced or acclimated stimulation of A has been mechanistically and quantitatively attributed to decreased maximum apparent carboxylation velocity (Vc,max) and investment in Rubisco (Rogers & Humphries, 2000). Photosynthetic acclimation is frequently reported along with an accumulation of leaf nonstructural carbohydrates and a decrease in N concentration in the leaf and plant (Stitt & Krapp, 1999; Nowak et al., 2004). Plant growth in elevated [CO2] in FACE experiments resulted in significant acclimation of C3 photosynthesis (Fig. 5). Vc,max was reduced on average by 13%, and the maximum rate of electron transport (Jmax) was reduced by 5%. There was also a significant 5% shift (reduction) in the ratio of Vc,max : Jmax. It has long been recognized that as CO2 rises, metabolic control of light-saturated photosynthesis by Rubisco (Vc,max) is decreased, and control by the rate of regeneration of RubP is increased (Jmax) (Long & Drake, 1992). Along with acclimation of photosynthetic capacity, there were significant reductions in Rubisco content and N content, measured on an area basis. Simultaneously, sugar and starch were increased substantially with growth under elevated [CO2] (Fig. 5). Variation in acclimation was apparent; functional groups showed different responses and the environmental conditions also altered acclimation.

image

Figure 5. Mean response of maximum carboxylation rate (Vc,max), maximum rate of electron transport (Jmax), ratio of Vc,max : Jmax, Rubisco content (mass/unit area), nitrogen content reported on both area and mass basis, chlorophyll content reported on both area and mass basis, sugar and starch content reported on area basis, ±95% CI. Number of species, FACE experiments and individual observations for each response are given in Appendix 2.

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1. Functional groups and FACE sites

The magnitude of photosynthetic acclimation differed between C3 functional groups. Vc,max tended to be reduced to a greater extent in grasses and shrubs than in trees and legumes (Fig. 6). At the FACTS 1, PopFACE, SoyFACE and New Zealand sites, Vc,max was not significantly changed under elevated [CO2] (Appendix 2). Jmax was significantly reduced in C3 grasses, and there was no significant downregulation of Jmax or N (measured on an area basis) in trees and legumes (Fig. 6). Why would trees and legumes have different responses from other functional groups? The N-fixing ability of legumes generally enhances their response to elevated [CO2] (Hebeisen et al., 1997; Lüscher et al., 1998, 2000). In the SoyFACE experiment, non-nodulating soybeans showed downregulation of Vc,max in elevated [CO2], while nodulating varieties maintained the same photosynthetic capacity under ambient and elevated [CO2] (Ainsworth et al., 2004). Lüscher et al. (2000) demonstrated the importance of N2-fixing capacity in the Swiss FACE experiment with effectively and ineffectively nodulating Medicago sativa. Under elevated [CO2], effectively nodulating M. sativa strongly increased harvestable biomass and N yield, while ineffectively nodulating plants were negatively affected by FACE. However, at the New Zealand FACE experiment photosynthetic acclimation was stronger in the two N-fixing species than in the grass species (von Caemmerer et al., 2001).

image

Figure 6. Comparative acclimation responses of different C3 functional groups to elevated [CO2]. Results from: ○, this meta-analysis; ◆, a prior meta-analysis of European tree species (Medlyn et al., 2001). Number of species, FACE experiments and individual observations for each response are given in Appendix 2.

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Downregulation of photosynthetic capacity in trees in response to FACE is highly variable. Medlyn et al. (1999) reported a similar decrease in Vc,max for European forest species; however, they also reported a significant 12% decrease in Jmax for field-grown tree species under elevated [CO2] (Fig. 6). Much of the data for trees included in this meta-analysis came from the Duke FACE experiment, where both loblolly pine and understorey hardwood species were examined (Ellsworth et al., 1995; DeLucia & Thomas, 2000; Naumburg & Ellsworth, 2000; Singsaas et al., 2000; Herrick & Thomas, 2001; Rogers & Ellsworth, 2002). DeLucia & Thomas (2000) reported that for four understorey hardwood tree species acclimation of photosynthesis did not involve any decrease in Vc,max or Rubisco, but leaves had increased capacity for RubP regeneration, which increased their ability to utilize sunflecks. These results were reflected in this meta-analysis, where Jmax was significantly increased and Vc,maxJmax was significantly decreased at the FACTS 1 site (Appendix 2). In the POPFACE experiment, downregulation of Vc,max was reported only in the slowest growing of the three poplar clones, Populus alba, which probably had the smallest sink capacity (Hovenden, 2003). Sink capacity may also explain variable downregulation of Vc,max in Populus tremuloides in the Rhinelander FACE experiment. Only mid- and lower-canopy leaves showed significant downregulation of photosynthetic capacity, while upper-canopy leaves with close proximity to rapidly growing sinks did not show any change in photosynthetic capacity (Takeuchi et al., 2001).

2. Nitrogen

Acclimation of photosynthesis to elevated [CO2] has been reported to be more pronounced when plants are N-limited, and to be absent when N supply is adequate (Stitt & Krapp, 1999; Isopp et al., 2000). Inadequate N supply could restrict the development of new sinks and therefore exacerbate the source–sink imbalance in plants grown under elevated [CO2] (Stitt & Krapp, 1999; Hymus et al., 2001). The results from the FACE experiments support this hypothesis. Under low N conditions there was a 22% decrease in Vc,max, and under high N conditions there was only a 12% decrease in Vc,max (Fig. 6). Nitrogen reported on an area basis was reduced 12% in plants grown under low-N conditions and elevated [CO2], but was not changed under unstressed conditions (Appendix 2).

Another explanation for accentuated acclimation under low-N conditions is that the decrease in Rubisco may reflect a general decrease in leaf protein caused by reallocation of N to younger leaves or earlier leaf senescence in N-limited plants (Stitt & Krapp, 1999). However, the results from the FACE experiments suggest that the decrease in Rubisco is specific, and not part of a general decrease in leaf protein. There was no change in chlorophyll content when measured on an area basis (Fig. 5). Assuming Rubisco to account for 25% of leaf N (Spreitzer & Salvucci, 2002), the 20% decrease in Rubisco could account for all of the 5% decrease in leaf N.

V. Growth, above-ground production and yield

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

Growth and above-ground biomass production generally increased with exposure to elevated [CO2]; however, the magnitude of the response varied between species, growing seasons and experimental conditions. Elevated [CO2] resulted in taller plants with larger stem diameter, increased branching and leaf number (Fig. 7). Surprisingly, stimulation of plant height with elevated [CO2] was greater in the third growing season than in the first and second (Appendix 2). Leaf-area index (LAI) was not significantly affected by growth at elevated [CO2], although this varied with functional group. Specific leaf area decreased 6% in plants exposed to elevated [CO2], although this trend also varied with plant functional group and species. One largely unanswered question in forest ecosystems is whether biomass production will be increased along with the increase in photosynthesis (Karnosky, 2003). Our results showed greater allocation to wood and structure in woody plants and a 28% increase in above-ground dry matter production for trees grown under elevated [CO2] (Fig. 8). Crop yield increased on average by only 17% (Fig. 7), considerably lower than previous estimates of crop yield increase in chambers (Kimball, 1983; Cure & Acock, 1986; Amthor, 2001; Jablonski et al., 2002).

image

Figure 7. Mean response to elevated [CO2] of plant height, stem diameter, leaf number, leaf-area index (LAI), specific leaf area (SLA), above-ground dry matter production (DMP), and crop yield. Number of species, FACE experiments and individual observations for each response are given in Appendix 2.

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image

Figure 8. Comparative responses to elevated [CO2] of different functional groups and experimental conditions on growth and yield variables. Results from: ○, this meta-analysis; ▪, a meta-analysis of tree species (Curtis & Wang, 1998); ▴, a meta-analysis of C4 grasses (Wand et al., 1999). ▾, comparative results from a meta-analysis of 79 crop and wild species (Jablonski et al., 2002). Number of species, FACE experiments and individual observations for each response are given in Appendix 2.

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1. Growth and leaf area

Plant height increased 14% in the third year of exposure to elevated [CO2], but was not affected in the first 2 yr of exposure (QB = 19.954, P < 0.001; Appendix 2). This result contrasts with the expectation that initial stimulation of growth in response to elevated [CO2] will diminish over time, possibly because of modifications in biomass allocation and phenology (Ward & Strain, 1999). Plant height increased more in shrubs and trees than C3 crops (Fig. 8). Thus those FACE experiments with trees and shrubs (FACTS 1, Rhinelander, PopFACE and NV Desert FACE) showed significant increases in plant height, while Maricopa and Rapolano showed no change in plant height (Appendix 2). Stem diameter increased 9% on average, and was unaffected by length of exposure to elevated [CO2]. Increased stem diameter was significantly affected by stress. Populus tremuloides grown under elevated [CO2] and increased [O3] showed a marginal 5% increase in stem diameter. Branch number was not highly reported in the FACE literature, but the limited results from six species at three FACE sites suggested an increase of 25% (Fig. 7). These results are consistent with those from a recent review of tree responses to elevated [CO2], where a persistent growth response and increased branching were reported (Saxe et al., 1998).

Overall, for 12 species in seven FACE experiments, leaf number was increased by 8% with growth at elevated [CO2] (Fig. 7). On average, LAI did not change with growth in elevated [CO2], but again this response varied with functional type. Trees had a 21% increase in LAI, but herbaceous C3 grasses did not show a significant change in LAI (Fig. 8). Trees have increased stem diameter and plant height, which allows for more leaves, either by more stems or greater hydraulic conductance per stem. The increase in LAI in trees could result in more rapid canopy closure, which would affect light interception (Ward & Strain, 1999) and potentially increase tree density in mixed grass/tree systems such as savanna and woodland ecosystems (as modeled by Bond et al., 2003). The OzFACE experiment in tropical savanna in Yabula, Australia should help answer questions about mixed grassland/woodland dynamics. Results from the Rhinelander experiment (reviewed by Karnosky et al., 2003) suggest that while elevated [CO2] increases LAI in P. tremuloides, ozone stress reduces LAI. Therefore when both CO2 and O3 are elevated there is no change in LAI (Karnosky et al., 2003).

2. Above-ground dry matter production

Above-ground dry matter production increased 20% on average for 29 C3 species grown in six different FACE experiments (Fig. 8). The increase in C3 biomass with elevated [CO2] is consistent with the increase in C3 plant mass reported by Jablonski et al. (2002) (Fig. 8). There was no change in dry matter production for the five C4 species measured at the Maricopa FACE experiment and the BioCON FACE experiment, and neither C4 crops nor C4 wild grasses showed any dry matter production stimulation with growth at elevated [CO2] (Fig. 8).

Stimulation of dry matter production differed between functional groups (Table 2; Fig. 8). Trees showed the largest response in dry matter production (28%), followed by legumes (24%; Fig. 8). C3 grasses only showed a 10% increase in above-ground production (Fig. 8). Curtis & Wang (1998) reported a 28.8% increase in total biomass for primarily young or juvenile trees grown under elevated [CO2] (≈ 700 ppm) in mostly chamber or glasshouse conditions. This suggests that either forests saturate their response at approximate 550 ppm, or the response of trees in FACE experiments differs from the that in growth chamber and glasshouse experiments. Trees grown under nutrient limitation had a nonsignificant 14% stimulation in above-ground biomass, although this is based on only four studies. The increase in legume production is less than that reported in two earlier meta-analyses for soybean biomass (Ainsworth et al., 2002) and legume biomass (Jablonski et al., 2002); however the CO2 concentration in FACE experiments is lower than the average CO2 concentration of most growth chamber and glasshouse experiments. The response of C3 grasses is substantially lower than the 38% increase in above-ground biomass of C3 Poaceae species reported by Wand et al. (1999). However, many of the data for our study come from the BioCON experiment and the low-N treatment at the Eschikon FACE experiment. The response of above-ground biomass to elevated [CO2] is limited under low-nutrient conditions in wild C4 grasses (Wand et al., 1999).

3. Crop yield

The average crop yield stimulation of 17% is lower than previous estimates of CO2 effects on crop yield, which ranged from 28 to 35% (Kimball, 1983; Cure & Acock, 1986; Amthor, 2001; Jablonski, 2002; Kimball et al., 2002). One explanation of the difference is that FACE experiments have not elevated [CO2] above 600 ppm. However, as a curvilinear increase with increase in [CO2] is projected, this value is less than expected from chamber studies. Of the four crops analyzed in this meta-analysis, only cotton, a woody crop, showed a significant yield enhancement with growth at elevated [CO2]. The stimulation in cotton yield with growth at elevated [CO2] was 42% on average. Mauney et al. (1994) found that the primary effect of FACE on cotton was to sustain the initial rate of boll loading in cotton for a longer period. The increased yield is also attributable to more rapid leaf development before fruiting, greater number of flowers, and sustained fruiting for a longer period (Mauney et al., 1994).

Wheat and rice also showed trends towards increases in yield, but these increases were not statistically significant (Fig. 8). The trend of ≈ 15% increase in wheat yield is in agreement with the estimates of Amthor (2001) and Jablonski et al. (2002). Sorghum yield was not affected by growth at elevated [CO2]. The sorghum data were taken from the Maricopa experiment where sorghum was grown under both wet and dry conditions (Ottman et al., 2001). Ottman et al. (2001) reported that sorghum yield was increased in elevated [CO2] under dry, but not under wet, conditions. The meta-analysis reflected these interactions between growth environment and elevated [CO2] (Fig. 8; Table 2). The yield under FACE conditions with no reported stress was 40%; however that result was based on only five observations. Under wet conditions, there was no increase in yield with elevated [CO2], and under dry conditions there was a 28% increase in yield (Appendix 2). Low N fertilization also eliminated any yield response to elevated [CO2] (Appendix 2).

VI. So, what have we learned?

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

To date, only two large-scale replicated FACE facilities have reported elevated [CO2] effects on yields of C3 food crops, wheat and rice. Both these grains have shown overall smaller increases than were expected based on earlier enclosure studies. Over 3 yr of growth, rice seed yield was increased by 7–5% in elevated [CO2] (Kim et al., 2003). Spring wheat yield increased only by 8% in two growing seasons (Kimball et al., 1995). These FACE experiments elevated [CO2] by ≈ 200 ppm above current ambient, whereas the average increase was 350 ppm in the chamber studies surveyed by Kimball (1983). If a linear response of yield to elevated [CO2] is assumed, then the expected yield increase that would have been predicted in these FACE studies, based on the earlier enclosure studies, is ≈ 19%. Further, this 19% is probably a minimum, as it is expected that increase in production with increase in [CO2] will show diminishing returns. For example, in open-top chambers grain yield of wheat (cv. Minaret) increased 27% on elevation of [CO2] from 359 to 534 ppm, but only a further 3% increase was observed when comparing plants grown at 649 to 534 ppm (Fangmeier et al., 1996). A similarly smaller than predicted response has recently been reported for soybean grown at elevated [CO2] within the SoyFACE experiment (Morgan, 2004).

This discrepancy has wide importance as the chamber values have formed the basis for projecting global and regional food supply, and the stimulation attributed to elevated [CO2] has commonly been presumed to offset yield losses that would otherwise result from increased stresses, including higher temperature, elevated ground-level ozone and changes in soil moisture. For example, an integrated assessment of Hadley Center (HadCM2) climate-change impacts on agricultural productivity in the contiguous USA predicted climate change for 2090 would diminish wheat yields in most of the northern US wheat belt in the absence of any direct effect of elevated [CO2] (Izaurralde et al., 2003). When the direct effects of elevated [CO2] are added, the combined effect that is simulated is an increase in yields. However, a 33% yield increase caused by increasing [CO2] by 350 ppm is assumed (Izaurralde et al., 2003). If chamber experiments have overestimated the direct effect of increased [CO2], this would have a major impact on projections of future crop yields and wider implications for extrapolations from chamber studies to terrestrial ecosystems in general.

Could the lower than expected values in FACE be a flaw of the technology? Because of the difficulty of control in the absence of wind and the cost of CO2, most of the FACE systems do not elevate CO2 at night. Elevated [CO2] has been suggested to inhibit dark respiration; however, re-evaluation of the methods used to measure dark respiration under elevated [CO2] suggests that this apparent effect was an artifact of earlier measurement systems, and is absent when these artifacts are eliminated (Amthor, 2000; Jahnke, 2001; Davey et al., 2004; Long et al., 2004). Using young tropical trees, Holtum & Winter (2003) recently showed that high-frequency fluctuations in [CO2] of the type produced by FACE technology may diminish the response of photosynthesis to elevated [CO2]. However, this seems an unlikely explanation of the lower than expected stimulation in the FACE crop experiments. First, Hendrey et al. (1997) found no difference between constant and fluctuating elevated [CO2] on whole-chain photosynthetic electron transport in wheat, provided that oscillations had a half-cycle of 30 s or less, which would include most of the fluctuations observed in FACE systems. Second, large fluctuations in [CO2] are also observed in open-top chambers (McLeod & Long, 1999), which account for much of the database on effects of elevated [CO2] on yield (Ainsworth et al., 2002). Third, trees, in contrast to crops, showed greater increases in production than predicted from chamber studies.

The general conclusions from this meta-analysis and a measure of our certainty around them are summarized in Table 3. Functional groups differed in their response to FACE. Trees were generally more responsive than grass, forbs, legumes and crops, showing an average 47% stimulation in Asat. The degree of photosynthetic acclimation was low, and the increase in leaf carbohydrates was also less than the increase for other functional groups. Trees also showed a significant increase in LAI, while there was no change in LAI in crops and grasses grown under FACE. Trees also showed the largest stimulation in dry matter production. While it may be surprising that trees responded more than herbaceous species, it is important to keep in mind that, for the most part, the trees grown under FACE conditions are young and rapidly growing. Nevertheless, in contrast to chamber studies, trees have been grown to canopy closure and to 6–20 m in height. Only with long-term exposure to FACE will the affect of elevated [CO2] on mature trees be revealed. At present, the indication is that the response is larger than anticipated from chamber studies. C4 species have shown a far smaller response in FACE than predicted by chamber studies. Most significant is that the decrease in N, often assumed to lead to an expected diminution of the response of vegetation to elevated [CO2] in the long term, is only marginal in FACE. Nitrogen per unit leaf area was decreased by only 5% (Fig. 5), and this could possibly be explained by the loss of Rubisco alone. The many large differences between the findings within FACE and prior chamber experiments (Table 3) clearly show the need for a wider use of FACE, and most importantly side-by-side experiments to separate technique from site difference. The greater responses of trees to CO2 in FACE than in chambers, and the lesser responses of crops in FACE relative to chambers, show two urgent needs. More extensive FACE experimentation with the major crops and within the major growing zones will allow better forecasting of the future food supply, given that predictions currently based on chamber experiments appear very optimistic. Similarly, longer-term FACE experiments with forests where responses may have been underestimated will be critical. FACE experiments with tropical forests, which remain completely unrepresented despite representing 50% of C in terrestrial biomass, are an obvious need. The much smaller reduction in N observed in FACE relative to chamber studies also requires some rethinking of effects of elevated [CO2] on N limitation and terrestrial biogeochemical models of future N and C cycles. Lack of a response in LAI to elevated [CO2] in all functional types, except trees, similarly suggests a need for adjusting current models that are being used to project future vegetation. Future FACE experiments should also consider multiple levels of elevated [CO2], ranging from 50 ppm above current ambient to double current ambient [CO2]. This would allow more accurate scaling of physiological results and validation of ecosystem models. Finally, while large-scale FACE plots provide the most realistic mimic of a future elevated CO2 atmosphere, they nevertheless have their limitations. While allowing far larger treatment plots than other technologies, a forest FACE ring still has a diameter close to the maximum height of its trees at maturity. This limits the potential for studying interactions with other environmental changes within the plot. Ever-decreasing prices of control hardware, improved control algorithms, and judicious placement near cheap or free sources of CO2 should allow the development of much larger release arrays that could elevate CO2 over much larger areas or provide controlled CO2 gradients. There is therefore a need to improve the technology as well as to maintain and, in some areas, expand FACE.

Table 3.  Comparison of the general results of plant responses to elevated [CO2] from this analysis of large-scale FACE experiments (FACE) vs previous quantitative reviews of elevated [CO2] experiments (prior)
GeneralityFACEPriorCertainty
Order of C3 functional group  responsivenessTrees > legumes > C3 grassesLegumes1 > grasses2 > woody plants3Low
 No difference in functional groups4 
C3 vs C4 responseC3 >> C4C3 > C45Low
C3 ≈ C42  
Sustained increase in carbon uptakeYesYes4,8High
No5  
Acclimation of photosynthesisVc,max/JmaxNo change in Vc,max/Jmax4,6High
Decrease in leaf NSpecific to and accounted for by RubiscoDilution effect6,8Medium
Increase in leaf-area indexTrees onlyYes7Low
No8  
Stimulation in crop yieldSmallLarge9,10Medium

Acknowledgements

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

This work was supported in part by the Terrestrial Ecosystem Response to Atmospheric and Climatic Change (TERACC) project headed by Dr Lindsey Rustad, which is supported with funds from the US National Science Foundation (DEB-0090238). E.A.A. was supported in part by the Alexander von Humboldt Foundation. We thank Victoria Wittig for her comments on the draft manuscript.

References

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

Appendices

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices

Appendix 1. References included in the database for meta-analyses

  1. Top of page
  2. Abstract
  3. I. What is FACE?
  4. II. Materials and methods
  5. III. Photosynthetic carbon uptake
  6. IV. Acclimation of photosynthesis
  7. V. Growth, above-ground production and yield
  8. VI. So, what have we learned?
  9. Acknowledgements
  10. References
  11. Appendices
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  • Gielen B, Scarascia-Mugnozza G, Ceulemans R. 2003. Stem respiration of Populus species in the third year of free-air CO2 enrichment. Physiologia Plantarum 117: 500507.
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  • Gunderson CA, Sholtis JD, Wullschleger SD, Tissue DT, Hanson PJ, Norby RJ. 2002. Environmental and stomatal control of photosynthetic enhancement in the canopy of a sweetgum (Liquidambar styraciflua L.) plantation during 3 years of CO2 enrichment. Plant, Cell & Environment 25: 379393.
  • Hacour A, Craigon J, Vandermeiren K, Ojanpera K, Pleijel H, Danielsson H, Hogy P, Finnan J, Bindi M. 2002. CO2 and ozone effects on canopy development of potato crops across Europe. European Journal of Agronomy 17: 257272.
  • Hamerlynck EP, Huxman TE, Nowak RS, Redar S, Loik ME, Jordan DN, Zitzer SF, Coleman JS, Seemann JR, Smith SD. 2000. Photosynthetic responses of Larrea tridentata to a step-increase in atmospheric CO2 at the Nevada Desert FACE facility. Journal of Arid Environments 44: 425436.
  • Hamerlynck EP, Huxman TE, Charlet TN, Smith SD. 2002. Effects of elevated CO2 (FACE) on the functional ecology of the drought-deciduous Mojave Desert shrub, Lycium andersonii. Environmental and Experimental Botany 48: 93106.
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Appendix 2. Results of the meta-analysis of FACE effects

Table 4. Results of the meta-analysis of FACE effects on light-saturated CO2 uptake (Asat), diurnal carbon assimilation (A′), apparent maximum quantum yield of CO2 uptake (AQY), stomatal conductance (gs), ratio of intercellular (ci) to atmospheric CO2 concentration (ca), instantaneous transpiration efficiency (ITE), maximum carboxylation rate (Vc,max), maximum rate of electron transport (Jmax), ratio of Vc,max : Jmax, Rubisco content, N content, chlorophyll content, sugar content, starch content, plant height, stem diameter, branch number, leaf number, leaf-area index, specific leaf area, crop yield and above-ground dry matter productio
VariableInteractionCategorydfNumber of speciesNumber of FACE sitesEffect size (E)Lower CIUpper CI
Asat  32645111.3111.2791.344
C3 vs C4C329740111.3371.3041.371
C4 28 5 31.1061.0241.194
FACE site (C4)BioCON 11 3 0.9820.8861.089
Maricopa 11 1 1.1961.0891.313
SoyFACE  4 1 1.1470.9321.41
Temperature (C3)<25°C 31 4 41.1851.0991.278
= 25°C22132111.2991.2631.336
Functional group (C3)Tree12612 51.4741.4251.524
Shrub 18 3 11.2111.0721.367
Grass 62 5 31.3631.2991.43
Forb 16 5 21.1481.0421.264
Legume 29 6 31.2071.1291.29
Crop (high N) 11 2 21.3651.2221.525
Stress (C3)None16828111.3561.311.403
Ozone 12 1 11.5921.3811.836
Low N 5515 31.2751.21.354
FACE site (C3 grasses)BioCON 12 4 1.1551.0361.288
Eschikon 50 3 1.411.3551.468
FACE site (Legume)BioCON  9 3 1.0760.9811.179
Eschikon  7 1 1.3671.2131.541
SoyFACE 11 1 1.2231.1341.32
A  14516 61.2841.2411.339
C3 vs C4C314215 61.2941.251.339
C4  5 1 11.070.8451.355
Functional group (C3)Tree 19 5 21.2861.1771.405
Shrub 29 3 11.4621.3311.605
Grass 39 2 21.3731.2841.468
Legume  6 1 11.2291.0361.459
FACE siteRhinelander  9 1 1.0210.91.16
Duke  2 1 1.6480.4765.705
NV Desert 34 5 1.4251.3221.537
PopFACE  9 3 1.5551.3531.787
Maricopa 43 2 1.1921.1311.256
Eschikon 38 1 1.3661.2821.454
SoyFACE 12 2 1.1621.0481.287
AQY   20 8 31.1221.0341.215
FACE siteRhinelander  3 1 1.0850.9231.275
Duke 11 4 1.2551.1731.344
PopFACE  6 3 0.980.881.091
gs  23440120.80.7740.827
Functional groupTree 78 6 30.8410.7950.891
Shrub 41 4 10.8840.8090.965
C3 grass 16 6 30.7780.6840.884
C4 grass 11 3 10.7510.620.909
Forb 16 3 10.8130.7170.922
Legume 24 4 30.7710.6930.858
SiteRhinelander 12 1 0.8030.7040.916
Oak Ridge 27 1 0.7730.6970.858
Duke 15 6 0.8290.7020.98
NV Desert 44 6 0.880.8090.959
PopFACE 21 3 0.9950.8861.119
Rapolano  5 4 0.8030.7040.916
BioCON 4612 0.7590.7040.819
Maricopa 33 3 0.7020.5350.922
Eschikon 16 6 0.6670.6060.734
SoyFACE 12 2 0.8340.7310.952
StressNone14535100.8460.8110.883
Low N 3712 30.7050.6450.769
Ozone  6 1 10.80.6440.995
Drought  6 1 10.5970.450.793
ci : ca   4712 70.9810.9611.001
SiteOakRidge  2 1 1.0190.6391.625
NV Desert  6 1 1.0010.9451.06
Rapolano  7 4 1.0190.9721.067
Eschikon 14 4 1.0180.9811.055
Maricopa 18 1 0.9330.9070.959
ITE   34 7 41.5431.381.726
C3 vs C4C3 28 6 31.681.5491.883
C4  5 1 11.0620.826.366
Functional groupTree 26 4 31.7371.5991.887
C3 grass  3 1 11.2580.7532.103
C4 grass  5 1 11.0690.841.361
Vc,max  22725 90.8690.8440.893
Functional group (C3)Tree 7111 40.9390.8930.988
Shrub 19 4 10.8220.7280.928
Grass 97 3 20.8290.7930.868
Legume 17 3 30.8780.7870.979
SiteDuke 29 7 0.9410.8781.009
PopFACE 29 3 0.9390.8691.017
NV Desert  8 6 0.890.8030.987
Eschikon 14 6 0.8290.7970.864
SoyFACE  6 1 0.8970.7361.093
New Zealand  6 3 0.750.5721.069
EnvironmentUpper canopy 8014 70.9020.860.946
Lower canopy 14 3 40.8780.7710.993
Understorey 17 6 10.9990.8781.137
Old 10 7 30.8760.7581.013
Young 11 7 30.9470.8151.106
NitrogenLow N 63 5 40.7760.7340.82
High N 48 4 40.8790.8260.935
Jmax  16719 80.9510.9260.977
Functional group (C3)Tree 57 9 40.9950.9551.038
Grass 72 2 30.9220.8880.958
Legume 17 2 20.9360.8621.017
SiteDuke 33 5 1.0891.0251.159
NV Desert  7 3 0.8050.6780.956
PopFACE 28 3 0.9650.9121.02
Eschikon 79 5 0.9140.8810.949
SoyFACE  5 1 0.9910.8551.147
New Zealand  5 3 0.7790.561.086
StressNone 8417 70.9950.9581.033
Low N 39 4 30.8860.8390.935
Vc,max : Jmax   9619 80.9510.9260.977
Functional group (C3)Tree 6111 40.9680.9470.99
Shrub  7 2 11.0540.9831.131
Legume 16 3 30.9450.9120.979
Rubisco content (mass/unit area)   23 6 30.8060.6920.94
N (mass/unit area)  12321 70.9510.9260.977
Functional groupTree 36 3 31.020.9781.065
Forb 12 1 30.8450.7810.914
Legume 14 6 20.9030.851.046
C3 grass 22 4 30.940.8771.009
C4 grass 13 4 20.9820.8771.113
SiteRhinelander  8 1 0.9480.8571.049
OakRidge  6 1 0.9870.8871.098
Duke 28 2 1.0310.9811.083
BioCON 4513 0.9050.8630.949
Japan 17 1 0.9180.8590.982
Eschikon  6 1 1.020.8921.167
New Zealand  7 3 0.8360.7410.944
StressNone 61 9 50.990.9571.024
Low N 3116 40.8790.8290.931
EnvironmentUpper canopy 20 3 31.0631.0021.127
(trees)      
Lower canopy 17 3 30.9610.9011.025
N (mass/mass)   99 5110.8680.8360.901
Functional groupTree 53 6 30.8990.870.93
Shrub  5 2 10.8520.7520.966
C3 grass  8 1 10.8820.8070.964
C3 crop 30 2 10.8190.7850.854
N (% dry mass)   32 4 30.8710.8380.906
StressNone 19 4 30.9230.8890.958
Ozone 14 2 10.8090.770.849
Chlorophyll (mass/unit area)   39 7 30.9690.9291.011
Chlorophyll (mass/mass)   31 6 30.8310.730.947
Chlorophyll a : chlorophyll b   19 6 31.0581.0051.115
Sugar (mass/unit area)   30 4 41.3191.1791.476
Functional group StressTree 10 2 21.1140.9011.377
Legume  7 1 11.4271.0811.884
None 18 3 31.2251.0771.393
Dry  5 1 11.71.2992.225
Wet  5 1 11.260.9621.65
Starch (mass/unit area)   30 4 41.8441.6152.104
Functional group SiteTree 10 2 21.3731.11.715
Legume  7 1 11.8421.3982.426
OakRidge  6 1 1.3120.9821.754
Duke  3 1 1.5390.8442.808
Maricopa 11 1 2.2871.9012.755
SoyFACE  7 1 1.8421.3672.429
StressNone 18 3 31.5541.3271.82
Dry  5 1 12.5191.863.41
Plant height   5810 51.0661.0431.089
Functional group SiteTree 44 4 21.061.0351.085
Shrub  8 2 11.2381.1231.361
Rhinelander 33 1 1.0531.0231.085
PopFACE  9 3 1.0751.0261.127
Rapolano  4 3 1.0130.9191.115
NV Desert  8 2 1.2411.1281.365
Maricopa  3 2 1.1080.9091.35
Growing season1 1410 51.0350.9981.071
2 16 6 41.03411.068
3 12 6 31.1381.0931.185
Stem diameter   53 6 31.0921.0661.119
StressNone 34 6 31.1151.0811.15
Ozone 20 1 11.0491.0041.096
Branch number   12 6 31.2471.0521.478
Leaf number   4412 71.0751.0451.106
SiteRhinelander  5 1 1.0210.9331.116
Desert  5 1 1.2251.0291.459
Eschikon 11 4 1.3941.2431.563
Leaf-area index   5311 61.0670.9991.142
Functional groupTree 15 6 31.2111.0441.404
C3 grass 10 1 11.1030.921.323
Specific leaf area  11324 60.9410.920.963
C3 vs C4C310220 60.9250.9080.952
C4 12 2 41.0250.9591.096
Functional groupTree 56 5140.9160.8860.947
Forb 12 1 30.9440.8761.017
Legume 10 1 30.9910.9171.072
C3 grass 24 2 40.9250.8840.968
C4 grass 12 1 31.0260.961.095
SiteDuke 41 6 0.9030.870.936
PopFACE  7 3 0.9660.8921.046
BioCON 4513 0.9820.9521.012
Eschikon 11 1 0.8960.840.956
Dry matter production  17434 61.171.1451.196
C3 vs C4C313029 61.1981.1711.226
C4 11 5 21.0360.9631.115
Functional groupTree  9 7 21.281.0641.541
C4 crop  6 1 11.0670.9781.166
C3 grass 41 8 31.1051.0651.148
C4 grass  3 4 10.9630.8041.154
Legume 18 6 31.2031.1371.273
SiteRapolano  4 3 1.2881.1071.498
Maricopa 27 3 1.2051.1461.268
Eschikon 55 7 1.1561.1131.201
Japan 17 1 1.2161.1411.296
BioCON 4616 1.1181.0711.166
New Zealand 14 6 1.2861.1151.482
Crop yield   27 6 31.1731.1021.249
SpeciesSorghum 11  11.0480.971.132
Cotton  6  11.4221.2371.636
Wheat  4  11.1440.9841.331
Rice  5  11.1040.9361.302
StressNone  4  1.4041.1391.731
Wet conditions  7  1.0510.9551.156
Drought  7  1.2771.1431.426
Low N  3  1.0840.7701.527
Main effects of FACE in bold font, along with degrees of freedom for each analysis and number of species and FACE sites that the analysis included.
Different categorical groups or interactions were tested further. The between-group heterogeneity (QB) across categorical variables and statistical significance of significant categorical differences are reported (e.g. the first categorical test determined the difference in the response of Asat between C3 and C4 species).