Introduction

The carbon dioxide (CO2) concentration has increased from ~ 280 to ~ 415 ppm in the atmosphere due to fossil fuel consumption, deforestation, and land-use changes1,2,3,4,5. The Intergovernmental Panel on Climate Change (IPCC) stated that by 2100, CO2 levels might reach the 1300 ppm mark2 and consequently increase the global temperature, needing mitigation alternatives to restrain climate change. The IPCC's 2021 report provides valuable insights into the potential impacts of elevated CO2 concentrations on plants, which can significantly improve plant growth and development. It highlights the need for further research to understand better the complex interactions between CO2 and other climate change factors and their effects on plant physiology, growth, and ecosystem functioning5.

One of the manners to capture the CO2 is forest maintenance and planting trees for carbon assimilation and biomass accumulation6. The increase in CO2 concentration stimulates photosynthesis, resulting in a productivity gain and more carbon storage7,8,9,10,11.

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 increase2,6,12,13,14,15,16,17,18. The increase in CO2 concentration can stimulate photosynthesis in plants; consequently, the stimulation is influenced by various processes such as carboxylation and product synthesis19. The rate of photosynthesis can be controlled by Rubisco, which is sensitive to CO2, and other less sensitive components19. In maize leaves, eCO2 concentration decreased whole-leaf chlorophyll and protein content20. The stomatal index was also significantly increased in plants grown at high CO2 concentrations20. Furthermore, eCO2 reduced transpiration and water consumption in tomato plants, increasing water use efficiency21 and decreasing leaf transpiration rates22. The increase in leaf dark respiration can result from the direct instantaneous effect of increased CO2 concentration and the longer-term indirect effect due to changes in leaf composition23. The increased carbon assimilation resulting from elevated CO2 concentrations has enhanced different crop species' growth, productivity, and biochemical constituents24. In leguminous plants, eCO2 concentrations have increased chlorophyll, total starch, sucrose, and total carbohydrate content25.

Exposure to eCO2 can lead to various biochemical changes in plants, including photosynthesis, respiration, chlorophyll content, and starch accumulation26. Yelle et al.27 investigated the acclimation of tomato plants to eCO2, which observed an accumulation of starch in the chloroplasts. This suggests that starch alone can not fully explain the loss of photosynthetic efficiency in eCO2-grown plants. To understand the biological adaptations to abiotic stress, such as eCO2, it is important to select crops to verify their impact on plant development26.

Several publications have widely identified changes in these parameters so that large amounts of data can be compiled to provide panels for understanding the climate change effect on plants. One way to analyze and summarize the data is meta-analysis, which affords a comparative analysis of several eCO2 experiments displaying the diversity of plant responses according to life habits such as trees and herbs15,28. 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 planet29,30 and also the future changes in agriculture and food production31,32.

The available data, including meta-analyses, is overwhelmed with temperate climate species6,12,13,18,28,33,34,35, lacking data from tropical (cultivated/exotic or native) plants6,28,35,36,37,38 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 America39, with tropical and subtropical plants allocating 52% of the carbon on Earth's surface to biomass storage6,35.

A recent meta-analysis about productivity and its potential for crop adaptation under eCO2 included a single study from Brazil with coffee trees35. However, considering that Brazil represents one of the primary sources of food on the planet40 and is also the world's largest area of tropical rainforest35, representing one of the hot spots of biodiversity in the world, it would be essential to include studies performed in the region to obtain a general and accurate view of the effects of CO2 elevation for food production and biodiversity.

Plants in elevated CO2 environments in neotropical regions are of great interest due to their importance for understanding the response of these plants to changes in atmospheric conditions. Levy-Varon et al.41 investigated how symbiotic nitrogen fixation influences the tropical forest carbon sink. They found that planted trees can double carbon accumulation early in succession and increase total carbon in mature forests by approximately 10%. It is important to consider the diversity of functional plant communities in understanding the carbon sequestration potential of neotropical plants at eCO2. Rull and Vegas-Vilarrúbia42 performed simulations involving all known vascular flora of the neotropical Guayana Highlands and predicted the potential extinction of approximately 80% of species due to global warming by the end of this century. Despite these studies, there is still a gap in knowledge about the response of neotropical plants to elevated CO2. Studies about the effects of eCO2 on Brazilian plants have been carried out in the last couple of decades16,43,44,45,46, and it has been recently pointed out that such data remain a gap in meta-analysis works42.

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) with the hypothesis that trees and herbs would respond differently to elevated CO2 concentrations.

Results

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

The eCO2 increased plants' assimilation rate by 44% (Fig. 1; Table 1). Overall, trees + herbs responses in biomass showed an average increase of 20% in leaves, 41% in stems, and 43% in roots (Fig. 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 Fig. 3. However, only total soluble sugars and starch content showed an increase of 7% and 47%, respectively (Fig. 3; Table 1).

Figure 1
figure 1

Responses of photosynthetic variables: Net CO2 assimilation (A), stomatal conductance (gs), dark respiration (Rd), foliar transpiration (E), water use efficiency (WUE), intercellular/ambient CO2 rate (Ci/Ca), maximum electron transport rate (Jmax), and maximum Rubisco carboxylation rate (Vcmax) according to life habits: Trees (a), Herbs (b), and Overall (c) in plants grown in elevated CO2. The circles represent the percentage changes in elevated CO2. Error bars represent 95% confidence intervals. Study numbers for each variable are shown in parentheses.

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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 Intervals (CI). Bold letters represent significant differences (p < 0.05).
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Figure 2
figure 2

Biomass responses in each plant organ (leaf, stem, root, grain, and total) in plants grown into elevated CO2 according to life habits: Trees (a), Herbs (b), and Overall (c). The circles represent the percentage changes in elevated CO2. Error bars represent 95% confidence intervals. Study numbers for each variable are shown in parentheses.

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Figure 3
figure 3

Responses of non-structural carbohydrates (glucose, fructose, sucrose, total soluble sugars, and starch) in plants grown to elevated CO2, according to life habits: Tree (a), Herbs (b), and Overall (c). The circles represent the percentage changes to elevated CO2. Error bars represent 95% confidence intervals. Study numbers for each variable are shown in parentheses.

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Elevated CO2 effect in trees and herbs according to life habits

The life habits were essential to distinguish responses in total biomass, stomatal conductance (gs), transpiration foliar (E), water use efficiency (WUE), and maximum rate of electron transport (Jmax) (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%) (Fig. 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 (Fig. 2; Table 1). The grain biomasses were only measured in herbs, which had no alteration in plants cultivated under eCO2 (Fig. 2). Starch increased by 61% in trees, while in the herbs, the fructose, sucrose, and soluble sugars increased by 13%, 15%, and 14%, respectively (Fig. 3; Table 1). When trees and herbs were analyzed separately, the assimilation increased by 39% and 52%, respectively (Fig. 3; Table 1). Stomatal conductance negatively affected herbs (p = 0.001; Table 2; Fig. 1). The reduction of gs (39%) in herbs increased WUE (117%) (Fig. 3). Thus, the photosynthesis parameters WUE, E, and Jmax differed among herbs and trees at eCO2 (Fig. 1; Table 2). These results may reflect a tendency for the opposite effects of these variables in trees and herbs (Fig. 1; Table 1). On the other hand, the trees displayed no significant effect in gs, WUE, and E at eCO2 (Fig. 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 (Figs. 1, 4). The lack of effect could reflect the small number of observations in those variables (Fig. 5), which calls for more studies to provide consistent analysis for these variables.

Table 2 Meta-analyses result in 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 the column in publication bias, the p-value < 0.05 does not indicate publication bias. For heterogeneity, analyses were considered I2 ≤ 25 low, I2 > 25 to 75 moderate, and I2 > 75 high heterogeneity.
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Figure 4
figure 4

Responses of potential quantum efficiency of photosystem II (Fv/Fm), total chlorophyll content, and proteins in plants grown in elevated CO2, according to life habits: Trees (white), Herbs (gray), and Overall (black). The circles represent the percentage change in elevated CO2. Error bars represent 95% confidence intervals. Study numbers for each variable are shown in parentheses.

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Figure 5
figure 5

Observation numbers from the literature extracted were divided into biomass, biochemical, and photosynthesis components according to life habits: Trees (black) and Herbs (gray) in experiments with elevated CO2. The variables correspond to total biomass, total soluble sugars, starch, proteins, net CO2 assimilation (A), stomatal conductance (gs), foliar 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 (total Chl) maximum Rubisco carboxylation rate (Vcmax), and maximum electron transport rate (Jmax).

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Heterogeneity and publication bias analysis

Heterogeneity (I2) analysis in the analytical models was used to evaluate the variation in results among observations. 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, Jmax, total chl, starch, and proteins (Table 2). High heterogeneity shows that external factors may influence the variation of the estimated effects among observations. The Vcmax showed moderate heterogeneity, and the Fv/Fm had low heterogeneity (Table 2). These results demonstrate less variation among observations in Vcmax and Fv/Fm variables.

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).

Discussion

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 growth15,47. 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). The elevated CO2 in plants through photosynthesis is directly connected to their growth and productivity48. In addition, elevated CO2 stimulated photosynthetic assimilation in neotropical herbs, improving WUE due to stomata closure and conductance reduction (Fig. 1). This behavior corroborates evidence reported in other meta-analyses12,28, except that neotropical trees did not alter the stomatal conductance responses as happens in temperate trees13.

Figure 6
figure 6

Tropical climate trees and herbs responses to elevated CO2.

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Stomatal conductance (gs) and assimilation rates control the intercellular/ambient CO2 ratio, which dictates the internal carbon allocation in plants49. Elevated CO2 increases the concentration of intracellular CO2 in leaves38, but to continue the assimilation, the mesophyll CO2 needs to display lower concentrations than the atmospheric partial pressure of CO250. This regulation is performed by the closure and opening of the stomata, which leads to a decrease in stomatal conductance38,51.

It has been reported that European forests grown in eCO2 decreased Jmax and Vcmax by 10%52. The authors attributed this decrease to the limiting levels of nitrogen in leaves. The Neotropical species examined in the present work did not decrease Jmax and Vcmax 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.53, the Vcmax parameter displays relevant implications for large-scale modeling. Carbon flux models show that simulated photosynthetic rates are particularly susceptible to Vcmax and Jmax, with the former being pointed out by Bonan et al.53 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 respiration, which may increase or decrease, depending on the species, when plants are exposed to unfavorable conditions54. 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 gain55,56. Thus, the efficiency of the carbon metabolism increases 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 trees12. However, no meta-analysis has been performed considering sugar metabolism and photosynthesis, so temperate and neotropical species could not be directly compared via meta-analysis.

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 carbohydrates19,57,58. 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 carbohydrates59. Starch is composed of insoluble and long-term storage polysaccharides (amylose and amylopectin) that are not readily available to participate in plant metabolic processes60 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 growth61. Furthermore, stimulation of photosynthesis with eCO2 had a response in the biomass increase different in the development of organs and plant seed mass62. Li et al.63 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 species13,47,52. However, in Brazil, relatively few experiments were carried out with eCO2 in plants from the biomes Pantanal, Caatinga, Cerrado, Amazon, and the Pampas, the latter in a temperate region (Table 3). Thus, more profound exploration should provide relevant information on how different biomes could answer to eCO2 and climate change64,65. Also, establishing long-term experiments to test the effect of eCO2 on plants over time in Brazil is needed once a significant portion of the neotropical plants is located there. This would allow an understanding of the physiological responses to climate change66.

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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Native plants in neotropical regions have evolved to adapt to their specific environmental conditions, including CO2 levels. Elevated CO2 can positively affect native plants by increasing photosynthesis, promoting plant growth, increasing carbon sequestration, and potentially acting as a CO2 sink16. In contrast, plants grown in neotropical regions are often grown for agricultural purposes. They may have different responses to eCO2 compared to native plants, although this hypothesis needs to be checked in further studies with more species. Cultivated plants can exhibit increased photosynthetic rates and grow under elevated CO235. This can benefit crop productivity and potentially increase carbon sequestration in farming systems67. However, the response of cultivated plants to elevated CO2 may vary depending on factors such as plant species, nutrient availability, management practices, and genetic improvement techniques68. Therefore, it is important to note that the potential of native and cultivated plants to act as CO2 sources or sinks is influenced by several factors. These include the specific plant species, their physiological characteristics, duration of exposure to elevated CO2, and general ecosystem dynamics. To understand the potential of native and cultivated plants in neotropical regions as sources or sinks of CO2, more research is needed.

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, rapidly growing. 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 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.

Conclusion

The responses of species native or cultivated in the neotropics to eCO2 can be attributed to contrasting growth strategies and physiological features of trees and herbs. Trees display greater carbon sink capacity and can allocate more resources for growth and storage. The higher rates of photosynthesis in response to eCO2 (39%) led to greater starch storage (61%) and a more significant biomass accumulation in tree organs (Table 1). This behavior may be attributed to the tree’s long lifespan and ability to allocate resources for growth and storage.

In contrast, herbs, which display shorter lifespans, prioritize rapid growth and reproduction and tend to allocate resources that would support higher water use efficiency (117%) due to decreased stomatal conductance (− 39%) under conditions of eCO2. Herbs responded differently, increasing net CO2 assimilation (52%) and soluble sugars such as sucrose and fructose (14%, 15%, and 13%). Understanding these responses would be crucial to predicting the impacts of increased CO2 levels on different types of plants in the face of eCO2 increases.

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 global climate change. Thus, more experiments are needed using these parameters that, together with modeling work, could help understand how the neotropics, with their rather large proportion of world biodiversity, will respond to climate change in this century.

Materials and methods

Data collection

For data collection, a systematic review was performed. A systematic review is a technique that selects primary studies on a given subject69. 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 reproducible69. The flowchart with steps for data collection is shown in Supplementary 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)70,71,72. For each database, a combination of keywords was used (Supplementary Table 1) that recovered 2096 works on the eCO2. In addition, 35 studies were manually included from leading Brazilian researchers by Lattes search (https://lattes.cnpq.br)72. Lattes is a Brazilian platform for integrating Curriculum, Research Groups, and Institution databases into a single information system72. The search resulted in a total of 2127 analyzed works in the systematic review (Supplementary Fig. 1). A database was assembled with 68 studies published before October 1st, 2021 (see Table 3; Supplementary 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 28 and 16 species, respectively (Table 3). The collected data were extracted in three theoretical categories: growth (biomass), biochemical (total 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 (Vcmax), and maximum rate of electron transport (Jmax)]. The biomass data were collected from total biomass or biomass per plant organ. Each biomass result per organ was considered a biomass observation. Each soluble sugar (glucose, fructose, sucrose, raffinose, and myoinositol) was considered an observation for the biochemical category. A dataset contemplated a total of 437 observations. In general, the duration of the studies was 90 days. The average high CO2 concentration was from ~ 400 to ~ 800 ppm. Fifty studies were performed in Open Top Chambers (OTC), 13 in Free Air CO2 Enrichment (FACE), and 7 in Glasshouse (GC). 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. Fourteen variables were analyzed [A, gs, E, WUE, Rd, Ci/Ca, biomass, total soluble sugars, starch, proteins, Fv/Fm, total Chl, Vcmax, Jmax] (Fig. 5). The most frequent variables were biomass (79), with 46 observations for trees and 33 for herbs (Fig. 5). From the total species analyzed, 30% represent cultivated ones. Among the trees, 21% are cultivated, and 79% are native species. Among herbs, 33% are native, and 67% are cultivated. 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 and Wang13 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 v4.173 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)74. Data from temporal experiments were considered only the last harvest to represent the maximum exposure of these plants to eCO2 cultivation.

Meta-analysis

Meta-analysis assessed 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 group68. The natural log of the response ratio (lnRR = X̅t/X̅c) was used and is reported as the mean percentage change [(lnRR − 1) × 100]75. 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 control76. The effect was reported as a percentage change from the control: ((elnRR − 1) × 100). In addition, life habits were used as a fixed predictor variable while the 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 species77,78. Furthermore, heterogeneity (I2) was tested to verify the variation in results between studies77,79. The Egger regression test was used to identify publication bias80,81. Bias analyses for the multilevel models were conducted with meta-analytic residuals77. Analyzes were performed using the package "metafor"82, and the graphics were generated using the package "ggplot2"78, both in R version program 3.6.083.