Meta-analysis of the responses of Brazilian trees and herbs to elevated CO 2

doi:10.21203/rs.3.rs-2604847/v1

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Meta-analysis of the responses of Brazilian trees and herbs to elevated CO 2

https://doi.org/10.21203/rs.3.rs-2604847/v1

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published 22 Sep, 2023

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The CO₂ concentration has increased in the atmosphere due to fossil fuel consumption, deforestation, and land-use changes. Brazil represents one of the primary sources of food on the planet and is also the world's largest tropical rainforest, which is one of the hot spots of biodiversity in the world. In this work, a meta-analysis was conducted to compare several CO₂ Brazilian experiments displaying the diversity of plant responses according to life habits, such as trees and herbs. We found that trees and herbs display different responses. The young trees tend to allocate carbon - from increased photosynthetic rates and lower respiration in the dark - to organ development, increasing leaves, roots, and stem biomasses. In addition, more starch is accumulated in the young trees, denoting a fine control of carbon metabolism through carbohydrate storage. Herbs increased drastically in water use efficiency, controlled by stomatal conductance, with more soluble sugars, probably with a transient accumulation of carbon primarily stored in seeds as a response to elevated CO₂.

Biological sciences/Biochemistry

Biological sciences/Plant sciences

Earth and environmental sciences/Climate sciences

Earth and environmental sciences/Environmental sciences

The carbon dioxide (CO₂) concentration has increased from ~ 280 ppm to ~ 415 ppm in the atmosphere due to fossil fuel consumption, deforestation, and land-use changes [1, 2, 3, 4, 5]. The Intergovernmental Panel on Climate Change (IPCC) stated that by 2100, CO₂ levels might reach the 1300 ppm mark [2] and consequently increase the global temperature, needing mitigation alternatives to restrain climate change.

One of the manners to capture the CO₂ is forest maintenance and planting trees to carbon assimilation and biomass accumulation [6]. The increase in CO₂ concentration stimulates photosynthesis, resulting in a productivity gain and more carbon storage [7, 8, 9, 10, 11, 12].

The photosynthesis parameters affected when plants grow under elevated CO₂ (eCO₂) are the reduction in stomatal conductance, leaf dark respiration rate, transpiration rate, maximum Rubisco enzyme carboxylation rate, and maximum transport of electrons rate that results in carbon assimilation increase [2, 6, 13, 14, 15, 16, 17, 18, 19]. Researchers have widely recorded changes in these parameters so that large amounts of data can be compiled to provide panels for understanding the climate change on plants.

One way to analyze and summarize the data is meta-analysis, which affords a comparative analysis of several CO₂ experiments displaying the diversity of plant responses according to life habits such as trees and herbs [16, 20]. Performing meta-analyses with data on leaf photosynthesis of forest trees and crops is important because such data are essential for modeling the future of carbon storage and sequestration on the planet [21, 22, 23] and also the future changes in agriculture and food production [24, 25].

The available data, including meta-analyses, is overwhelmed with temperate climate species [6, 13, 14, 19, 20, 26, 27, 28] lacking data from tropical plants [6, 20, 28, 29, 30, 31] and preventing more accurate analysis of some key regions containing high biodiversity and food production in the world. Contrasting to the high proportion of publications focusing on temperate species, about 43% of all Earth's tree species occur in South America [32], with tropical and subtropical plants allocating 52% of the carbon on Earth's surface to biomass storage [6, 20].

A recent meta-analysis about productivity and its potential for adaptation in crops under eCO₂ included a single study from Brazil with coffee trees [28]. However, considering that Brazil represents one of the primary sources of food on the planet [33, 34] and is also the world's largest area of tropical rainforest [35], representing one of the hot spots of biodiversity in the world, it would be essential to include studies performed in the region to obtain general and accurate view of the effects of CO₂ elevation for food production.

Studies about the effects of eCO₂ on Brazilian plants have been carried out in the last couple of decades [17, 36, 37, 38, 39, 40, 41] and it has been recently pointed out that such data remain as a gap in meta-analysis works [42].

This work aimed to perform a meta-analysis on the eCO₂ responses in plant physiological parameters in Brazilian climates, representing a relevant portion of the Neotropics. In these analyses, it was possible to: (I) estimate the size of the average effects of high atmospheric CO₂ on biomass, biochemical, and photosynthesis parameters and (II) verify whether the eCO₂ effects are influenced by the species' life habits (trees and herbs). It was found that trees and herbs respond differently to eCO₂. The former, with samples of young individuals mainly, tend to increase photosynthesis, leading to higher storage of starch and higher biomass accumulation in the organs. Herbs, consisting mainly of fast-growing crop plants, also increase net CO₂ assimilation but tend to increase water use efficiency and decrease stomatal conductance significantly.

2.1. Photosynthetic parameters, biomass, and starch increased in leaves of tropical plants under elevated CO₂

The eCO₂ increased plants' assimilation rate by 44% (Figure 1; Table 1). Overall, trees + herbs responses in biomass showed an average increase of 20% in leaves, 41% in stems, and 43% in roots (Figure 2; Table 1). The results in non-structural carbohydrates composed of glucose, fructose, sucrose, and starch present in the leaves of trees and herbs under CO₂ are shown in Figure 3. However, only soluble sugars and starch content showed an increase of 7% and 47%, respectively (Figure 3; Table 1).

2.2. Elevated CO₂ effect in trees and herbs according to life habits

The life habits were essential to distinguish responses in total biomass, A, gs, E, WUE, and J_max (Table 2). The biomass increase is different per organ between trees and herbs under eCO₂. The biomass increased more in trees than in the herbs category, being higher on leaves (194%), stems (245%), and roots (250%) (Figure 2; Table 1). In herbs, the biomass increased by 28% and 77% in stems and roots, respectively. Furthermore, changes in the biomass of leaves were not significant in herbs (Figure 2; Table 1). The grain biomasses were only measured in herbs, which had no alteration in plants cultivated under eCO₂ (Figure 2). Starch increased by 61% in trees, while in the herbs, the fructose, sucrose, and soluble sugars increased by 13%, 15%, and 14%, respectively (Figure 3; Table 1). When trees and herbs were analyzed separately, the assimilation increased by 39% and 52%, respectively (Figure 3; Table 1). Stomatal conductance negatively affected herbs (p= 0.001; Table 2; Figure 1). The reduction of gs (39%) in herbs increased WUE (117%) (Figure 3). Thus, the photosynthesis parameters WUE, E, and J_max differed among herbs and trees at eCO₂ (Figure 1; Table 2). Possibly, these results may reflect a tendency of the opposite effects of these variables in trees and herbs (Figure 1; Table 1). On the other hand, the trees displayed no significant effect in gs, WUE, and E at eCO₂ (Figure 1; Table 1). Under eCO₂, trees significantly reduced dark respiration (17%). Furthermore, Ci/Ca, Jmax, Vcmax, Fv/Fm, and total Chl in trees and herbs under eCO₂ did not change under eCO₂ (Figure 1; Figure 4). It is important to note that the lack of effect could reflect the small number of observations in those variables (Figure 5), which calls for more studies to provide consistent analysis for these variables.

2.3. Heterogeneity and publication bias analysis

Heterogeneity (I²) analysis in the analytical models was used to evaluate the variation in results among studies. The high heterogeneity indicates variation in the effect of eCO₂ among observations. The heterogeneity was high (I² > 75) for total biomass, A, gs, Rd, E, WUE, Ci/Ca, J_max, total chl, starch, and proteins (Table 2). High heterogeneity shows that external factors may influence the variation of the estimated effects among observations. The Vc_max showed moderate heterogeneity, and the Fv/Fm had low heterogeneity (Table 2). These results demonstrate that in the variables Vc_max and Fv/Fm, there is less variation among observations.

No publication bias was found for net CO₂ assimilation, dark respiration, foliar transpiration, water use efficiency, intercellular/ambient CO₂ rate, maximum carboxylation rate, the potential quantum efficiency of PSII total chlorophyll, and total soluble sugars (Table 2). However, the Egger test identified publication bias for biomass, gs, Jmax, and starch (Table 2).

Plants can be used to capture carbon to delay the effects of climate change through photosynthesis, which assimilates carbon in the form of CO₂ and accumulates it into the plant's biomass. Thus, higher carbon availability is expected to generate changes in these processes and intensify plant growth [16, 43]. In the meta-analysis presented in this work, data from species planted as crops and native species to the neotropics were examined. We confirmed previous literature observations regarding the physiology of temperate species, showing that several neotropical ones alter their photosynthesis parameters, biomass accumulation, and sugars (biochemicals) under eCO₂ (Fig. 6). In addition, elevated CO₂ stimulated photosynthetic assimilation in neotropical herbs, improving WUE due to stomata's closure and conductance reduction (Fig. 1). This behavior corroborates evidence reported in other meta-analyses [13, 20], except that neotropical trees did not alter the stomatal conductance responses for temperate trees [14].

Stomatal conductance (gs) and assimilation rates control the intercellular/ambient CO₂ ratio, which dictate the internal carbon allocation in plants [44]. Elevated CO₂ increases the concentration of intracellular CO₂ in leaves [31], but to continue the assimilation, the mesophyll CO₂ needs to display lower concentrations than the atmospheric partial pressure of CO₂ [45]. This regulation is performed by the closure and opening of the stomata, which leads to a decrease in stomatal conductance [31, 46].

It has been reported that European forests grown in eCO₂ decreased J_max and Vc_max by 10% [47]. The authors attributed this decrease to the limiting levels of nitrogen in leaves. The Neotropical species examined in the present work did not decrease J_max and Vc_max changes (Fig. 1), possibly indicating that the leaf nitrogen status in the experiments used for this meta-analysis was not limited. According to Bonan et al. (2011) [48], the Vc_max parameter displays relevant implications for large-scale modeling. Carbon flux models show that simulated photosynthetic rates are particularly susceptible to Vc_max and J_max, with the former being pointed out by Bonan et al. (2011) [48] as a model-dependent parameter. Therefore, accuracy in these parameters is critical for a more effective prediction and modeling by the global panels.

The sugars produced during photosynthesis can be metabolized for maintenance and developmental processes. Catabolism of sugars leads to the consumption of ATP by the respiration process, which may increase or decrease, depending on the species, when plants are exposed to unfavorable conditions [49]. When neotropical plant species were subjected to elevated CO₂ during growth, they displayed a decrease in dark respiration (Rd) (see Overall in Fig. 1), which is expected to increase the efficiency of the net productivity of carbon gain [50,51]. Thus, the efficiency of the carbon metabolism seems to increase under eCO₂. The decrease in Rd may be associated with the higher concentrations of foliar starch found in plants grown under eCO₂ analyzed in Overall (Table 1). The same pattern of reduction of Rd was observed for temperate trees [13]. However, no meta-analysis has been performed considering sugar metabolism and photosynthesis, so temperate and neotropical species could be compared.

An explanation for the higher accumulation of starch in leaves of neotropical species growing under eCO₂ is that the photosynthetic assimilation rate can exceed the growth capacity, leading to the accumulation of non-structural carbohydrates [52,53,54]. We found that starch increase (47%) represents the primary non-structural carbohydrate in plant leaves under eCO₂ (Fig. 2).

The increased starch levels in eCO₂ are usually the main element responsible for increasing the content of total non-structural carbohydrates [55]. Starch is composed of insoluble and long-term storage polysaccharides (amylose and amylopectin) that are not readily available to participate in plant metabolic processes [56] but can be used to increase biomass in leaves, stems, and roots, as observed in this meta-analysis (Fig. 2). The carbohydrates synthesized in leaves from extra CO₂ supply were translocated into tree stems (Fig. 2), suggesting that the reserve biomass is driven to this organ, boosting secondary growth [57]. Furthermore, stimulation of photosynthesis with eCO₂ had a response in the biomass increase different in the development of organs and plant seed mass [58]. Li et al. (2018) [59] synthesized 71 tree species and data of a more significant increase in starch than soluble sugars in leaves under eCO₂.

The results obtained in this work show that the responses of neotropical plant species to eCO₂ are consistent with those on the global scale (temperate climates mainly), suggesting that the predictions made by models of climate change would answer similarly to temperate and neotropical species [14,43.47]. However, in Brazil, relatively few experiments were carried out with eCO₂ in plants from the biomes Pantanal, Caatinga, Cerrado, and the Pampas, the latter in a temperate region (Table 3). Thus, more profound exploration should be made to provide relevant information on how different biomes could answer to eCO₂ and climate change [42, 60]. Also, establishing long-term experiments to test the effect of eCO₂ on plants over time in Brazil - where a significant portion of the Neotropics are - would allow an understanding of the physiological responses of plants in different climates to eCO₂ since vegetation responses to climate change seem to be tightly connected to long-term processes [61].

Figure 6 summarizes the responses of the neotropical species analyzed in this work. Temperate and neotropical species respond similarly to eCO₂, which is likely to reflect directly in the consistency of modeling regarding the adjustment of parameters. trees and herbs display different responses. The trees studied are primarily young and, therefore, at a rapid growth phase. As they are not yet at the reproductive stage, young trees tend to allocate carbon - from increased photosynthetic rates and lower respiration in the dark - to organ development, significantly increasing leaves, roots, and stem biomasses. As growth rates are somehow limited in comparison with the growth capacity of most herbs, more starch is accumulated in trees, denoting a tight control of carbon metabolism through carbohydrate storage. Herbs, mainly crop plants, reached reproductive maturity during the experiments. Their strategy to respond to eCO₂ involved a drastic increase in water use efficiency, controlled by stomatal conductance. In addition, the plants tend to display more soluble sugars, probably with a transient accumulation of carbon primarily stored in seeds.

Finally, it is essential to note that eCO₂ alone does not represent the complete response of plants to climate change. Combinations of eCO₂ with stresses of temperature and water will be necessary to assess the systemic response of plants to the global climate change. Thus, more experiments are needed using these parameters that, together with modeling work, could help understand how the neotropics, with their large proportion of world biodiversity, will respond to climate change in this century.

4.1. Data collection

For data collection, a systematic review was performed. A systematic review is a technique that selects primary studies on a given subject [62]. For the elaboration of the systematic review, it is necessary to identify and describe the steps taken to study selection and data extraction. These steps must follow a protocol that can be consulted and reproducible [62]. The flowchart with steps for data collection is shown in Supplemental Fig. 1. Literature search for the data collection on the effect of the elevated CO₂ on plants was performed in three databases: Web of Science, Scielo, and Brazilian Digital Library of Theses and Dissertations (https://bdtd.ibict.br) [63, 64, 65]. For each database, a combination of keywords was used (Supplemental Table 1) that recovered 2.096 works on the eCO₂. In addition, 35 studies were manually included from leading Brazilian researchers by Lattes search (https://lattes.cnpq.br) [66]. Lattes is a Brazilian platform for integrating Curriculum, Research Groups, and Institution databases into a single information system [66]. The search resulted in a total of 2.127 analyzed works in the systematic review (Supplemental Fig. 1). A database was assembled with 68 studies published before October 1st, 2021 (see Table 3; Supplemental Fig. 1). The included works were: (a) studies on Brazilian manipulative experimentation, reporting results from both the treatment groups (eCO₂) and the control groups (ambient CO₂ = aCO₂); (b) studies on trees or herbs; and (c) studies with the mean, sample size, and standard deviation of error of the selected variables. The data from articles were grouped as trees and herbs on 25 and 17 species, respectively (Supplemental Table 1; Table 1). The collected data were extracted in three theoretical categories: growth (biomass), biochemical (soluble sugars, starch, and proteins), and photosynthesis-related parameters [net CO₂ assimilation (A), stomatal conductance (gs), transpiration foliar (E), water use efficiency (WUE), dark respiration (Rd), intercellular/ambient CO₂ ratio (Ci/Ca), the potential quantum efficiency of PSII (Fv/Fm), total chlorophyll content (Chl), maximum carboxylation rate (Vc_max), and maximum rate of electron transport (J_max)]. The biomass data were collected from total biomass or biomass per plant organ. Each biomass result per organ was considered a biomass observation. For the biochemical category each soluble sugar (glucose, fructose, sucrose, raffinose, and myoinositol) was considered an observation. A dataset contemplated a total of 477 observations. In general, the duration of the studies was 90 days. The average high CO₂ concentration was from ~ 400ppm to ~ 700ppm. Fifty studies were performed in Open Top Chambers (OTC), 13 in Free Air CO₂ Enrichment (FACE), and 10 in Growth Chambers (CG). The most frequently studied species among trees was Coffea arabica, with 12 different studies. On the other hand, among herbs was Panicum maximum with six different studies. Thirteen variables were analyzed [A, gs, E, WUE, Rd, Ci/Ca, Fv/Fm, total Chl, Vc_max, J_max] (Fig. 5). The most frequent variables were biomass (79), with 46 observations for trees and 33 for herbs (Fig. 5). The experiments were considered unstressed unless the author had identified some stress factor. In the case of stress treatments, data from the control treatments were used. Most of the works had an average duration of experimentation of 90 days. The plants were grown in pots. Plants that received fertilizer treatment were not included in this analysis. The plants were watered regularly and exposed to natural light.

Observations of each study at the end of the experiment were grouped, and there was no categorization by experiment period. There was also the group for the elevated CO₂ levels of the different studies. Curtis & Wang 1998 [14] examines each subgroup for categorical divisions such as pot size and exposure time. However, a meta-analysis by these authors did not find significant differences among the groups by pot size and experiment time. This is an example that, throughout all studies, suggests significant differences in the response of plants under the CO₂ environment and, however, not among those grown in different pot sizes or experiment duration.

Mean values, standard deviation/error, and sample size under eCO₂ and aCO₂ were collected for each observation. WebPlotDigitizer v4.1 [67] was used to obtain the numerical data from the figures. For works that showed only the standard error value, the following equation was used: (SD = SE * √n) (n is the sample size, SE is the standard error, and SD is the standard deviation) [68]. Data from temporal experiments were considered only the last harvest to represent the maximum exposure of these plants to eCO₂ cultivation.

4.2. Meta-analysis

Meta-analysis was performed to assess plant responses to eCO₂ in growth, biochemical composition, and photosynthesis categories. To evaluate the relative changes of these responses between treatment (eCO₂) versus control (aCO₂), it was applied the logarithmic response ratio ln (RR), calculated as the size effect, where X̅t is the mean of the experimental/treatment group and X̅c is the mean of the control group [69]. The natural log of the response ratio (lnRR = X̅t/X̅c) was used, and is reported as the mean percentage change [(lnRR – 1) × 100] [69]. Values of lnRR higher than zero indicate that the eCO₂ effect increases, while negative values indicate that the eCO₂ effect decreases concerning aCO₂. A hierarchical mixed-effects model was used to estimate the mean and 95% confidence interval (CI) of the lnRR for each type of response variable. If the 95% CI of a response variable overlaps zero, the lnRR of the treatment is not significantly different from the control [70]. The effect was reported as a percentage change from control: ((e^lnRR − 1) *100). In addition, life habits were used as a fixed predictor variable, while study and species were considered random variables to control for the lack of independence of observations from the same study or/and carried out with the same plant species [71,72]. Furthermore, heterogeneity (I²) was tested to verify the variation in results between studies [71,73,74]. The Egger regression test was used for the identified publication bias was tested [75,76,77]. Bias analyses for the multilevel models were conducted with meta-analytic residuals [71]. Analyzes were performed using the package "metafor" [78], and the graphics were generated using the package "ggplot2" [79], both in R version program 3.6.0 [80].

ACKNOWLEDGEMENTS

We thank the Graduate Program in Bioinformatics from University of São Paulo – USP, São Paulo, Brazil for the finantial support.

FUNDING

This research was funded by the Instituto Nacional de Ciência e Tecnologia do Bioetanol-INCT do Bioetanol, grant numbers FAPESP 2014/50884-5 and CNPq 465319/2014-9 and Centro de Pesquisa e Inovação de Gases de Efeito Estufa—RCG2I (FAPESP/Shell 2020/15230-5). J.S.F. (CNPq 380198/2021-5). A.G. (FAPESP 2019/13936-0). D.P. (CAPES 88882.377113/2019-1).

CONFLICTS OF INTEREST

The authors declare no conflict of interest. The funders had no role in the study’s design, in the collection, analyses, or interpretation of the data; in the writing of the manuscript; or in the decision to publish the results.

Author Contributions

J.S.F., A.G., C.T.C., and M.S.B. conceived the study. J.S.F, D.P. and A.G. collected the data and conducted statistical analysis. All authors participated in the writing. M.S.B consolidated writing and produced the final version of the manuscript.

Data Availability

All data generated or analyzed during this study are included in this published article [Supplementary Table 2].

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Ghini, R., Torre-Neto, A., Dentzien, A.F.M. et al. Coffee growth, pest and yield responses to free-air CO2 enrichment. Climatic Change 132, 307–320 https://doi.org/10.1007/s10584-015-1422-2 (2015).
Godoy, J.R.L. Ecofisiologia do estabelecimento de leguminosas arbóreas da Mata Atlântica, pertencentes a diferentes grupos funcionais, sob atmosfera enriquecida com CO₂: uma abordagem sucessional. Thesis (Doutorado) -- Instituto de Botânica da Secretaria de Estado do Meio Ambiente (2007).
Grandis, A. Respostas fotossintéticas e de crescimento da espécie amazônica Senna reticulata sob elevada concentração de CO2. Dissertação de Mestrado, Instituto de Biociências, Universidade de São Paulo, São Paulo. doi:10.11606/D.41.2010.tde-18012011-171004 (2010).
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Tables 1 to 3 are available in the Supplementary Files section.

No competing interests reported.

Fortireretal2023Supplemental.docx
SupplementalTable2.xlsx
TABLE123.docx
Table 1. Meta-analysis with the percentage change of the biomass, photosynthesis, and biochemical variables measured in Trees and Herbs under elevated CO₂. Observation numbers (k). The effect size values are represented as Log response rate (LnRR) and percentage. Average estimates with lower and upper Confidence Interval (C.I.). Bold letters represent significant differences (p <0.05). Table 2. Meta-analyses results to different variables according to life habits: Trees and Herbs, publication bias, and heterogeneity. Bold letters represent significant differences between Trees and Herbs P≤0.05. For data from column in publication bias the p-value ≤0.05 no indicate publication bias. For heterogeneity analysis were considered I2 ≤ low, I2 > 25 to 75 moderate and I2 > 75 high heterogeneity. Table 3. Species found in a literature search with plants grown at different CO₂ atmospheric concentrations (ambient CO₂ = aCO₂ and elevated CO₂ = eCO₂), classified according to life habits: Tree and Herbs. OTC = Open Top Chambers, Face= Free Air Carbon Enrichment, and GC = Glasshouse. Ppm = parts per million.

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Meta-analysis of the responses of Brazilian trees and herbs to elevated CO 2

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