Biomass responses to intraspecific competition differ between wild species and CO2
1 Department of Biology, Indiana University–Purdue University Indianapolis, 723 West, Michigan Street, Indianapolis, IN 46202, USA
2 Department of Biological Sciences, Butler University, 4600 Sunset Avenue, Indianapolis, IN 46208, USA
* Correspondence address. Department of Biology, Indiana University-Purdue University Indianapolis, 723 West Michigan Street, Indianapolis, Indiana 46202, USA. E-mail: xzwang{at}iupui.edu
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Abstract |
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Aims: How growth of wild and crop species responds to global environmental perturbations has both ecological and agricultural significance in a changing world. The primary aim of this synthesis was to quantitatively assess the interactive effects of intraspecific competition and elevated CO2 on biomass production in herbaceous species.
Methods: Using meta-analytical techniques, we synthesized data from publications before 2006 that reported biomass responses to elevated CO2 in 321 herbaceous species grown in isolation or in competition with con-specific individuals.
Important findings: Intraspecific competition differentially modified biomass responses to elevated CO2 in wild and crop species. For example, competition reduced CO2 stimulation of total biomass (WT) from 27 to 23% in wild species, but by a much greater magnitude, i.e., from 43 to 32% in crops. Competition had no effect on responses of either above- (WAG) or below-ground (WBG) biomass to elevated CO2 in wild species, but significantly diminished CO2 enhancement of WAG, although not of WBG, in crops. Considerable variations were found among functional groups in the modification of growth responses to elevated CO2 by intraspecific competition, which exerted greater depression on CO2 enhancement in C3 than in C4 species and in non-legumes than in legumes. Elevated CO2 affected leaf and stem growth of individually grown C3 graminoids and forbs similarly, but increased leaf growth only in C4 graminoids and stem growth only in C4 forbs. Results from this synthesis demonstrated that intraspecific competition differentially affected growth responses to elevated CO2 in wild and crop species. The wild–crop species differences will have important implications for understanding primary production by herbaceous species in both natural and agricultural ecosystems in the future when atmospheric CO2 is significantly higher than the current level.
Keywords: biomass production • CO2 enrichment • functional groups • meta-analysis
Received: 19 September 2007 Revised: 11 December 2007 Accepted: 18 December 2007
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Introduction |
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Wild and crop species differ in a number of characteristics, most notably in the traits that have been selected for over time. Wild plant species have been naturally selected to maintain or increase their fitness under natural and mostly resource-limiting conditions, while crops have been selected by human beings during the last 10,000 years for fast growth and high productivity under agricultural and more favorable conditions (Simpson and Ogorzaly 1995). As a result, wild and domesticated species not only differ in physiology and growth under current conditions, but also respond differently to changing environments. One of the most significant environmental changes on a global scale is the steadily rising CO2 concentration in the atmosphere. It has reached 380 µmol mol–1, an unprecedented level for at least the last 420,000 years (Petit et al. 1999) and will likely approach 700 µmol mol–1 by the end of this century (Houghton et al. 2001). How growth of wild and crop species responds to elevated CO2 and other environmental perturbations will therefore have far-reaching implications for future primary productivity in both natural and agricultural ecosystems.
Because of the well-documented rise in atmospheric CO2 (Keeling et al. 1989) and its potentially significant effects on primary productivity, the last three decades have witnessed enormous efforts by the global change research community to learn more about plant growth in a higher CO2 environment, as evidenced by the large number of publications on this topic (Science Citation Index®). These studies have greatly advanced our understanding of effects of elevated CO2 on higher plants, particularly with regard to the direction of growth response to CO2. It is now a consensus that plant productivity will increase in response to higher CO2. The magnitude of increase, however, is much less certain, especially concerning growth responsiveness in wild and crop species. For example, an early review found significantly greater increase of biomass production at elevated CO2 in crops compared to wild species (Poorter 1993), but a recent meta-analysis detected no such differences (Jablonski et al. 2002). There were also large interspecific variations and a high degree of dependence on other environmental factors (Idso and Idso 1994; Kimball et al. 2002). These inconsistent responses found in different studies may be partly caused by the different nature and varying intensity of competition in different environments because competition has been shown to greatly modify growth response to higher CO2 (Bazzaz 1990; Bazzaz and McConnaughay 1992; Poorter and Navas 2003; Wang 2007). Since competition is common in all ecosystems, natural or agricultural, it is imperative that we improve our mechanistic understanding on plant growth response to elevated CO2 in environments differing in intensity of competition.
This meta-analysis was aimed at quantitatively assessing whether biomass production responded differentially to elevated CO2 in herbaceous species when grown individually or in competition with con-specific individuals. In an earlier synthesis, Poorter and Navas (2003) examined the modifying effects of competition on growth enhancement by elevated CO2 in a number of functional groups. In this study, we distinguished between wild and crop species because of the different growth traits that have been naturally or artificially selected for over their breeding histories. Examining differential growth responses to elevated CO2 in plants with different evolutionary traits when grown with or without intraspecific competition will undoubtedly improve our mechanistic understanding of global environmental changes on future primary productivity in ecosystems dominated by herbaceous species.
There were three specific objectives in this analysis: (i) to examine the effects of intraspecific competition on the overall effects of elevated CO2 on biomass production in wild and crop species; (ii) to compare growth responses to elevated CO2 between C3 and C4 and between leguminous and non-leguminous species grown in isolation or in competition with con-specific individuals and (iii) to quantify how CO2 enrichment affects leaf and stem biomass production in wild and crop species grown individually and if there was difference between graminoids and forbs. We only focused on herbaceous species because the majority of crops that have been studied for growth response to elevated CO2 are non-woody. A comparative examination between wild and crop species that are both herbaceous would therefore minimize the potential confounding effects of different growth forms, e.g., woody versus herbaceous species.
We hypothesized that responses to elevated CO2 would be less in wild species than in crops, especially at the individual level because crops have been repeatedly selected for their higher productivity under mostly favorable growth conditions in managed ecosystems. We further hypothesized a competition-dependent difference between C3 and C4 species and between legumes and non-legumes in responding to elevated CO2 because of their physiological differences in carbon and nitrogen acquisition. By differentiating responses to elevated CO2 in plants grown individually and in competition, our meta-analysis will be of particular relevance to a CO2 enriched and yet competitive environment as human beings turn to agro-ecosystems for food supply and to natural ecosystems for ecological services to meet the requirements of its rapidly increasing population.
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Database construction
Peer-reviewed journal articles used in building the database for this meta-analysis were obtained by searching the Science Citation Index®. Key phrases used in our searching included elevated CO2, CO2 enrichment, rising CO2, higher CO2, increasing CO2 and CO2 increase. The list of articles obtained was subsequently cross-checked with references cited in a large number of CO2 review articles and books to ensure inclusion of the greatest number of articles possible in the database. Any article published in English before 2006 that met the following requirements were included: (i) ambient CO2 treatments <400 µmol mol–1 and elevated CO2 treatments between 500 and 999 µmol mol-1; (ii) the entire plant exposed to CO2 treatments for the majority of the time period between emergence and harvesting for biomass determination and (3) reported responses of total biomass (WT), above-ground biomass (WAG), below-ground biomass (WBG), leaf biomass (WLF) or stem biomass (WST) to elevated CO2. The articles that reported growth change in percentages, but not absolute growth, were also included because it was the ratio of biomass at elevated to ambient CO2 that would be subjected to meta-analysis in this review. Because plants were exposed to a wide range of CO2 levels in different studies, the magnitude of CO2 increase in the elevated over ambient CO2 treatments for the response variables was presented in Table 1 to help data interpretation. Because of the little variations in ambient CO2 levels in the CO2 studies (typically between 350 and 370 µmol mol-1), the average magnitude of CO2 elevation shown in the table indicates the differential between the CO2 levels as well as the CO2 concentration for the elevated CO2 treatment.
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Plants were first grouped into wild and crop species and then into individual and population categories. A species that has both wild populations and cultivars was classified as a crop if a cultivar was identified in the publication. It was classified as a wild species if seeds were collected from a wild population for the empirical study. Plants grown individually included: (1) isolated plants grown in indoor environments or in pots placed inside chambers or Free Air CO2 Enrichment (FACE) rings in the field; (ii) plants grown hydroponically but no shading of one individual by another was intended or observed. Plants that were grown in close proximity of at least another con-specific individual in the same pot or in the field were defined as a population. Because the focus of this synthesis was to examine how absence or presence of intraspecific competition, rather than the intensity of competition, would modify growth responses to elevated CO2, we did not further categorize populations based on population density, which was not sufficiently reported in the majority of publications. Nutrient levels were not categorized because nutrients were typically oversupplied by researchers in most empirical studies to eliminate confounding of nutrient with CO2 effects, unless nutrient was a treatment itself. Any study that implemented a stress on the plants, such as limiting nutrient supply, high ozone or growth-limiting temperature, was excluded from this meta-analysis. Additionally, a simple quantification of the amount of nutrients supplied or sizes of pots used in the empirical studies would add little value because only the amount of nutrient supply dynamically integrated over the growth period of the plants could elucidate the interaction of nutrients and CO2 (Körner 2003). The advantage of meta-analysis over empirical studies and traditional reviews, however, is its ability to synthesize a large number of studies to reveal the overall effects of treatments. The categorization will allow us to adequately test the specific hypotheses, i.e., how intraspecific competition would modify effects of elevated CO2 on plant growth.
For this meta-analysis, only herbaceous species were analyzed for better comparison between wild and crop species because most crops that have been examined in CO2 studies are herbaceous and were typically exposed to experimental CO2 levels for the whole life cycles. For multi-season experiments, studies from all years were included for annual species, but only the studies with the longest CO2 exposure were included for perennial species. A single study could therefore contribute more than one independent observation (ratio of a variable at elevated to ambient CO2) to this database. Efforts were made to exclude duplicated results reported in multiple publications to maximize the uniqueness and independence of observations. In all, 554 publications that reported growth responses to elevated CO2 were included in our database. A list of the studies included and categorizations is available online at the website of the Journal of Plant Ecology or from the corresponding author upon request. From these publications, 3,064 observations were extracted for growth parameters. These observations were from studies on 278 species at the individual and 94 species at the population levels for a total of 321 unique herbaceous species.
Meta-analytical methods
The meta-analysis followed the techniques described in the work of Curtis and Wang (1998). We used log-transformed ratio of biomass at elevated to ambient CO2 (lnr) to estimate effect size of CO2 treatment (Hedges et al. 1999). In order to include the large number of studies that did not adequately report sample sizes and variances, we performed unweighted analysis using the statistical software MetaWin 2.0 (Rosenberg et al. 2000). Confidence intervals (CIs) on effect-size estimates were generated by bootstrapping the unweighted data using MetaWin 2.0 with a resampling of 9,999 iterations. Elevated CO2 was considered to have a significant effect on a variable if the CI of its response ratio did not overlap zero. Competition was considered to have a significant effect on a variable if the CIs of plants grown individually and in competition did not overlap (Gurevitch and Hedges 1993). Likewise, two functional groups were considered significantly different from one another if their CIs were non-overlapping. Significance was established at P < 0.05 level unless otherwise noted.
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Results |
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The magnitude of growth stimulation by elevated CO2 was highly dependent on competition in the environment and differed substantially between wild and crop species (Fig. 1). For example, intraspecific competition had no diminishing effect on CO2 enhancement of total biomass (WT) in wild species, but reduced WT enhancement from 43 to 32% in crops (Fig. 1a). Similarly, competition reduced responsiveness of above-ground biomass (WAG) to elevated CO2 only from 28 to 22% in wild species (ns, non-significant), but from 36 to 25% in crops (P < 0.01; Fig. 1b). Production of below-ground biomass (WBG) was not significantly affected by competition in either wild or crop species (Fig. 1c).
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Elevated CO2 increased WT in both C3 and C4 species, regardless of their breeding history (Fig. 2a and d). Intraspecific competition, though, differentially affected the magnitude of WT responses to elevated CO2 in herbaceous species with different photosynthetic pathways. For C3 species, competition had no significant effect on the magnitude of WT enhancement by elevated CO2 in wild species, but reduced WT stimulation in crops from 45 to 33% (P < 0.01; Fig. 2a). For C4 species, competition had no effect on WT enhancement in wild species, but surprisingly increased WT stimulation by elevated CO2 in crops (Fig. 2d). Higher CO2 increased WAG in C3 wild species, regardless of competition (Fig. 2b), but only in C4 wild species grown individually (Fig. 2e). Higher CO2 enhanced WAG in crops of both C3 and C4 photosynthetic pathways, whether they were grown individually or in competition (Fig. 2b and e). The magnitude of WAG stimulation was much greater in C3 than in C4 species and was dependent on the growth environment. For instance, competition reduced CO2 stimulation of WAG from 31 to 23% in C3 wild species (ns) and from 38 to 26% in C3 crops (P < 0.01; Fig. 2b), but had no diminishing effect on WAG in C4 species (Fig. 2e). WBG was found to respond differently from WAG to elevated CO2 and competition. In C3 species, elevated CO2 greatly increased WBG, but competition had no depressing effect on WBG responses in either wild or crop species (Fig. 2c). In C4 species, elevated CO2 had no effect on WBG in wild species (4%, ns), but increased WBG in crops grown in isolation (+11%; Fig. 2f). There were not sufficient studies to warrant valid assessment of WBG in C4 crops grown in monocultures.
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After analyzing the overall patterns of biomass production in C3 and C4 species, we further examined the growth responses to elevated CO2 and competition in wild graminoids and forbs grown with or without intraspecific competition. There were insufficient studies on cultivated forbs for comparison with graminoid crops. For C3 wild species, elevated CO2 increased biomass production, regardless of growth forms or competition (Fig. 3a–c). For C4 wild graminoids, growth enhancement by elevated CO2 was primarily manifested in WAG at both individual and population levels (Fig. 3e). For C4 forbs, WAG and WBG increased in response to elevated CO2 in plants grown in isolation (Fig. 3e and f). There were insufficient studies for examining C4 forbs grown in competition with con-specific individuals.
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Intraspecific competition greatly reduced the enhancing effect of elevated CO2 on WT in wild legumes, but not in crop legumes (Fig. 4a). Competition had no effect on WT or WAG in non-leguminous wild species, but significantly reduced stimulation of elevated CO2 on WT and WAG in non-leguminous crops (Fig. 4d and e). No diminishing effect of competition was found on WBG in non-leguminous wild or crop species (Fig. 4f). In all cases, elevated CO2 significantly increased production of WT, WAG and WBG in non-legumes, whether they were wild or crop species. For this analysis, C4 species were excluded from non-legumes, so the comparison was between legumes and non-legumes both with C3 photosynthetic pathway.
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Elevated CO2 increased leaf biomass (WLF) in both C3 and C4 wild species grown without intraspecific competition, although the magnitude of increase was much greater for C3 (+29%) than for C4 (+7%) species (Fig. 5a and b). In C3 species, leaf growth was enhanced significantly by elevated CO2, regardless of functional groups or ability for symbiotic N2 fixation. In C4 species, however, elevated CO2 only increased WLF in graminoids (Fig. 5b). Stem biomass (WST) responded to elevated CO2 similarly as WLF in C3 wild species, but differently in C4 species (Fig. 6). While elevated CO2 significantly increased WST in forbs (+14%), it had no effect on WST in graminoids (Fig. 6b).
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Discussion |
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Wild and crop species are two distinctive groups of plants that differ in a number of important ways, most notably in the traits that have been selected for over time. As a result, wild and crop species have been shown to respond differently to global environmental changes, such as elevated CO2 (Jablonski et al. 2002). Our meta-analysis on herbaceous species demonstrated that intraspecific competition differentially affected growth response to elevated CO2 in wild and crop species. Intraspecific competition reduced growth responses to elevated CO2 to a greater extent in crops than in wild species. Conversely, cultivated species grown in isolation responded significantly more to elevated CO2 than wild species grown in an environment in absence of intraspecific competition.
The greater depressing effect of competition on growth enhancement by elevated CO2 in crops than in wild species is presumably related to the different intensity of interaction among individuals at the population level in these two groups of plants. Crops have been selected over their breeding history for uniform sizes among individuals for easier harvesting. Consequently, crops have less size differentials than wild species when grown in monocultures. Size equality has been postulated as a major factor conducive to stronger plant–plant interactions and more intense competition (Bazzaz and McConnaughay 1992; Weiner 1985). The greater intensity of competition in crops grown in competition with con-specific individuals is therefore one likely reason that led to greater depression on growth by competition in response to elevated CO2.
In addition to being selected for more consistent sizes among individuals, crops have been bred for higher productivity and faster growth rate under relatively favorable but competitive conditions in agro-ecosystems. Wild species, on the other hand, have been naturally selected and are adapted to the conditions in unmanaged ecosystems, which generally have lower abundance of soil resources. When crops were grown in isolation and under mostly optimum conditions, such as controlled environments in most CO2 studies, crops may be able to better utilize the high resource availability and realize their greater growth potential than wild species. As a result, the wild–crop difference in growth responsiveness to elevated CO2 was much greater when plants were grown individually than when grown in monocultures.
It is noteworthy that the depressing effect of intraspecific competition on growth responses to elevated CO2 was manifested primarily in above-ground parts (Fig. 1). No significant reduction by competition was observed in below-ground growth, especially in crops. For instance, intraspecific competition reduced WAG in crops from 36 to 25%, but had no depressing effects on WBG (35 versus 38%). These results suggest that herbaceous crops would maintain or even increase biomass allocation to roots at the expense of shoot growth when grown in competition with other individuals of the same species because below-ground resources become relatively more limiting in a competitive and higher CO2 environment. The 25% increase in WAG by elevated CO2 found in this study, though, is consistent with an increase of 21% in crops grown in chambers (Kimball 1986) and an increase of 19% in a variety of C3 crops grown under field conditions (Kimball et al. 2002).
It has long been recognized that growth response to elevated CO2 in herbaceous species varies among functional groups, particularly in C3 and C4 species, because of their different physiology in carbon acquisition (Hunt et al. 1991; Idso and Idso 1994; Kimball 1983; Kimball et al. 2002; Nowak et al. 2004; Poorter 1993; Poorter and Navas 2003). Our meta-analysis showed the depressing effects of intraspecific competition also differed between C3 and C4 species. In C3 species, competition reduced total plant growth primarily through a reduction in above-ground growth. This effect was absent in C4 species. As a matter of fact, competition greatly increased the stimulating effect of elevated CO2 on total biomass of C4 crops. This surprising increase, however, might have been caused by the techniques used to raise CO2 concentration in different studies that were synthesized in this meta-analysis. Corn and sorghum, the only two C4 crops studied for response to elevated CO2 in the field, were grown in outdoor environments (chambers) in 5% of the individual-level studies, while 60% of the population-level studies were conducted in chambers or FACE experiments. Crops grown under field conditions were typically more water stressed than those grown in indoor chambers. Water stress has been shown to increase responsiveness to CO2, even though the absolute growth may be significantly lower (Acock and Allen 1985; Idso and Idso 1994; Kimball et al. 2002).
We further examined wild C3 and C4 herbaceous species by dividing them into graminoids and forbs because of their contrasting growth forms. The greatest difference between C3 and C4 species in responsiveness to elevated CO2 was found in WBG of graminoids. While WBG in C3 graminoids was significantly enhanced by elevated CO2, WBG in C4 graminoids was unaffected even when grown in competition with other individuals (Fig. 3f). The non-responsiveness of WBG to CO2 in C4 graminoids found in this analysis was largely due to the inclusion of five C4 species that were negatively affected by higher CO2. Below-ground growth was reduced by 22–41% in elevated compared to ambient CO2 grown Cynodon dactylon, Panicum coloratum, Panicum miliaceum, Pleuraphis rigida and Setaria feberii (Carlson and Bazzaz 1982; Ghannoum and Conroy 1998; Paterson et al. 1996; Yoder et al. 2000; Ziska et al. 1999). These species apparently had a large impact on growth responsiveness to elevated CO2 by the graminoids synthesized in this review. A meta-analysis, nonetheless, enables the integration of multiple studies and produces the overall responsiveness to elevated CO2. The wide range of WBG response to elevated CO2, in addition to the different leaf and stem growth responses in C4 graminoids found in this study, suggests that predicting productivity in ecosystems dominated by C4 graminoids could be more challenging than in other ecosystems.
Legumes differ from other plants in how nitrogen is acquired from the environment. Since nitrogen is one of the more limiting nutrients in natural and agricultural soils and therefore a resource that neighboring plants compete for, legumes and non-legumes may be affected differentially by competition in their growth response to elevated CO2. This is indeed what we found in this synthesis, although only in crops. Response of non-leguminous crops to CO2 enrichment was significantly depressed by competition, but the response of leguminous crops seemed unaffected. Since competition reduces plant growth primarily through reduction of resources availability to the individuals in a population, growth of legumes is less limited by N, most likely due to the symbiotic relationship of legumes with N2-fixing bacteria in the soil. Results from this analysis are consistent with those of Kimball et al. (2002), who found large growth increase in leguminous crops, regardless of soil nitrogen availability. Our findings provide additional support to the contention that competition diminished growth responsiveness to elevated CO2 in much the same way as low availability of soil nutrients, particularly N.
Despite the numerous advantages of a meta-analysis in research synthesis, caution should be exerted when interpreting meta-analytical outcomes. For any meta-analysis, the species that are easier to investigate in empirical studies may be over-represented in a synthesis. Over-representation will make the results of a review skewed and thus less representative, especially when the sample size is small. In order to gauge the impact of species over-representation on this meta-analysis, we conducted a sensitivity test and reanalyzed the observations by excluding Triticum aestivum and Glycine max, a non-legume and a legume well represented in CO2 studies and in this synthesis. With all the species included, elevated CO2 stimulated WT by 43.0% (n = 385) in crops grown in isolation and by 32.3% (n = 334) in crops grown in competition (Fig. 1a). When T. aestivum was excluded, elevated CO2 enhanced WT of individually grown crops and those grown with intraspecific competition by 44.4% (n = 336) and 32.8% (n = 266), respectively. When G. max was excluded, elevated CO2 enhanced WT of individually grown crops and those grown with intraspecific competition by 42.4% (n = 319) and 31.7% (n = 301), respectively. The little difference found in the sensitivity tests demonstrated that no single species, regardless of its ability for symbiotic N2 fixation, had disproportionate effect on the outcome of this meta-analysis. The high degree of robustness of this synthesis is apparently attributed to the large number of studies that were included in our analysis. Our tests highlight the importance of having a reasonable sample size in order to make meta-analytical results less skewed and thus more useful.
In summary, our meta-analysis revealed that CO2 stimulation of biomass production was differentially affected by intraspecific competition in wild and crop species. Magnitude of growth depression by competition also differed between C3 and C4 species and between legumes and non-legumes with different cultivation histories. Since intraspecific competition is ubiquitously present in both natural and managed systems, results from this meta-analysis will help improve our mechanistic understanding of the effects of CO2 enrichment on primary production by herbaceous species in the future.
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Supplementary Data |
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Supplementary material is available at Journal of Plant Ecology online.
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Acknowledgements |
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The authors thank Dr Bruce Kimball, Dr Leanne Jablonski and two anonymous reviewers for constructive comments and suggestions on an earlier version of this article. Financial support for this project was provided in part by the IUPUI Office of Professional Development. We thank the Interlibrary Loan Team at the IUPUI University Library for obtaining a large number of articles for this project. The technical support of Isaac Arthur, Alex Owusu-Agyeman, Ryan Jenkinson, Doug Latino, Riddhi Trivedi, Ly Vu and a number of other students is gratefully acknowledged.
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Acock B, Allen LH. Crop responses to elevated carbon dioxide concentrations. In: Direct Effects of Increasing Carbon Dioxide on Vegetation—Strain BR, Cure JD, eds. (1985) Washington, DC: U.S. Department of Energy. 53–97.
Bazzaz FA. The response of natural ecosystems to the rising global CO2 levels. Ann Rev Ecol Syst (1990) 21:167–96.[CrossRef][ISI]
Bazzaz FA, McConnaughay KDM. Plant-plant interactions in elevated CO2 environments. Aust J Bot (1992) 40:547–63.[CrossRef][ISI]
Carlson RW, Bazzaz FA. Photosynthetic and growth response to fumigation with SO2 at elevated CO2 for C3 and C4 plants. Oecologia (1982) 54:50–4.[CrossRef][ISI]
Curtis PS, Wang XZ. A meta-analysis of elevated CO2 effects on woody plant growth, form, and physiology. Oecologia (1998) 113:299–313.[CrossRef][ISI]
Ghannoum O, Conroy JP. Nitrogen deficiency precludes a growth response to CO2 enrichment in C-3 and C-4 Panicum grasses. Aust J Plant Physiol (1998) 25:627–36.[ISI]
Gurevitch J, Hedges LV. Meta-analysis: combining the results of independent experiments. In: Design and Analysis of Ecological Experiments—Scheiner SM, Gurevitch J, eds. (1993) New York: Chapman and Hall. 378–425.
Hedges LV, Gurevitch J, Curtis PS. The meta-analysis of response ratios in experimental ecology. Ecology (1999) 80:1150–6.[CrossRef][ISI]
Houghton J, Ding Y, Griggs D, et al. Climate Change 2001 (2001) Cambridge University Press.
Hunt R, Hand DW, Hannah MA, et al. Responses to CO2 enrichment in 27 herbaceous species. Funct Ecol (1991) 5:410–21.[CrossRef]
Idso KE, Idso SB. Plant responses to atmospheric CO2 enrichment in the face of environmental constraints: a review of the past 10 years research. Agric For Meteorol (1994) 69:153–203.[CrossRef]
Jablonski LM, Wang XZ, Curtis PS. Plant reproduction under elevated CO2 conditions: a meta-analysis of reports on 79 crop and wild species. New Phytol (2002) 156:9–26.[CrossRef][ISI]
Keeling CD, Bacastow RB, Carter AF, et al. A three-dimensional model of atmospheric CO2 transport based on observed winds: 1. Analysis of observational data. Geophys Monogr (1989) 55:165–236.
Kimball BA. Carbon dioxide and agricultural yield: an assemblage and analysis of 430 prior observations. Agron J (1983) 75:779–88.
Kimball BA. Influence of elevated CO2 on crop yield. In: Carbon Dioxide Enrichment of Greenhouse Crops Volume 2: Physiology, Yield, and Economics—Enoch HZ, Kimball BA, eds. (1986) Boca Raton, FL: CRC Press. 105–15.
Kimball BA, Kobayashi K, Bindi M. Responses of agricultural crops to free-air CO2 enrichment. Adv Agron (2002) 77:293–369.
Körner C. Nutrients and sink activity drive plant CO2 responses—a note of caution with literature based analysis. New Phytol (2003) 159:537–8.[CrossRef][ISI]
Nowak RS, Ellsworth DS, Smith SD. Functional responses of plants to elevated atmospheric CO2—do photosynthetic and productivity data from FACE experiments support early predictions? New Phytol (2004) 162:253–80.[CrossRef][ISI]
Paterson E, Rattray EAS, Killham K. Effect of elevated atmospheric CO2 concentration on C-partitioning and rhizosphere C-flow for three plant species. Soil Biol Biochem (1996) 28:195–201.[CrossRef]
Petit JR, Jouzel J, Raynaud D, et al. Climate and atmospheric history of the past 420,000 years from the Vostok ice core, Antarctica. Nature (1999) 399:429–36.[CrossRef]
Poorter H. Interspecific variation in the growth response of plants to an elevated ambient CO2 concentration. Vegetatio (1993) 104/105:77–97.[CrossRef]
Poorter H, Navas ML. Plant growth and competition at elevated CO2: on winners, losers and functional groups. New Phytol (2003) 157:175–98.[CrossRef][ISI]
Rosenberg NJ, Adams DC, Gurevitch J. MetaWin: Statistical software for meta-analysis. Version Version 2.0 (2000) Sunderland, MA: Sinauer Associates.
Simpson BJ, Ogorzaly MC. Economic Botany—Plants in Our World (1995) 742, 2nd edn. New York: McGraw-Hill, Inc.
Wang XZ. Effects of species richness and elevated carbon dioxide on biomass accumulation: a synthesis using meta-analysis. Oecologia (2007) 152:595–605.[CrossRef][ISI][Medline]
Weiner J. Size hierarchies in experimental populations of annual plants. Ecology (1985) 66:743–52.[CrossRef][ISI]
Yoder CK, Vivin P, Defalco LA, et al. Root growth and function of three Mojave Desert grasses in response to elevated atmospheric CO2 concentration. New Phytol (2000) 145:245–56.[CrossRef][ISI]
Ziska LH, Sicher RC, Bunce JA. The impact of elevated carbon dioxide on the growth and gas exchange of three C4 species differing in CO2 leak rates. Physiol Plant (1999) 105:74–80.[CrossRef]
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