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Hierarchical feedbacks of vegetation and soil carbon pools to climate constraints in Brazilian ecosystems

ABSTRACT:

It remains unclear whether temperature and precipitation exert independent control on tropical vegetation and soil C pools. Likewise, it is unknown whether the feedbacks of tropical C pools to climate constraints vary with nutrient availability. These aspects are critical to improving our ability to predict the response of tropical C pools to climate dynamics. This review aimed to assess climate data and the spatial distribution of vegetation and soil C pools across the Brazilian territory to investigate i) whether mean annual precipitation (MAP) and temperature (MAT) exert independent effects on tropical C pools; ii) whether vegetation and soil C pools exhibit hierarchical feedbacks to climate; and iii) how these feedbacks reflect soil nutrient availability. To account for MAP and MAT effects on tropical C cycling, we calculated Ecosystem Effective Moisture (EEM), i.e., the difference between MAP and potential evapotranspiration. We gathered substantial evidence suggesting that under high MAT and MAP controlling EEM, plants exchange more C for water and resorb more nutrients (especially P), which limitations in plant litter reduce microbial-derived C inputs into soil organic matter. Frequent soil saturation under high EEM favors denitrification rates (“open” N cycle), allowing continuous mineralization of litter and shallow soil C pools to release nutrients, sustaining high plant C pools. With decreasing MAP levels, ecosystem C pools depend on MAT controlling evapotranspiration and EEM. Accordingly, decreasing MAP under high MAT reduces EEM, with vegetation and soil C pools co-limited by low net primary productivity (NPP), frequent fire and/or nutrient losses. Otherwise, decreasing MAP and coupled to cool temperatures allow EEM to remain positive, forcing plants to increase deep-rooting and/or shed their leaves, which nutrients are immobilized with microbial-derived C into mineral-organic associations, favoring high soil C pools. Combined, the evidence gathered suggests that the sensitivity of tropical ecosystems to global increases in temperature should not be overlooked, especially if coupled to reductions in precipitation. Overall, the horizontal distribution of vegetation and soil C pools is best described by EEM rather than temperature or precipitation alone, whereas the vertical partition of C in plant-soil systems reflects biotic responses to climate-nutrient constraints.

Keywords:
tropical ecosystems; terrestrial C dynamics; soil-plant-atmosphere; ecosystem C stocks; nutrient cycling

INTRODUCTION

Mounting evidence suggests that rising atmospheric levels of CO2 increase the turnover rate of C in the plant-soil continuum even in the short-term ( van Groenigen et al., 2017van Groenigen KJ, Osenberg CW, Terrer C, Carrillo Y, Dijkstra FA, Heath J, Nie M, Pendall E, Phillips RP, Hungate BA. Faster turnover of new soil carbon inputs under increased atmospheric CO2. Glob Chang Biol. 2017;23:4420-9. https://doi.org/10.1111/gcb.13752
https://doi.org/10.1111/gcb.13752...
). In the long-term, rising CO2 levels also should cause climate changes, but our ability to predict their impacts on terrestrial C pools remains limited, particularly for tropical ecosystems ( Cavaleri et al., 2015Cavaleri MA, Reed SC, Smith WK, Wood TE. Urgent need for warming experiments in tropical forests. Glob Chang Biol. 2015;21:2111-21. https://doi.org/10.1111/gcb.12860
https://doi.org/10.1111/gcb.12860...
). Critically, the mean residence time (MRT) of tropical C pools (vegetation and soils combined) appears to be less than 20 years ( Carvalhais et al., 2014Carvalhais N, Forkel M, Khomik M, Bellarby J, Jung M, Migliavacca M, Μu M, Saatchi S, Santoro M, Thurner M, Weber U, Ahrens B, Beer C, Cescatti A, Randerson JT, Reichstein M. Global covariation of carbon turnover times with climate in terrestrial ecosystems. Nature. 2014;514:213-7. https://doi.org/10.1038/nature13731
https://doi.org/10.1038/nature13731...
). Given that tropical C fluxes are already high, it is critical to assess the extent to which environmental changes may impact the size of vegetation and soil C pools, which combined represent approximately 846.0 Pg carbon (1 Pg C = 1.0 × 1015 g C) at global scales ( Scharlemann et al., 2014Scharlemann JPW, Tanner EVJ, Hiederer R, Kapos V. Global soil carbon: understanding and managing the largest terrestrial carbon pool. Carbon Manag. 2014;5:81-91. https://doi.org/10.4155/cmt.13.77
https://doi.org/10.4155/cmt.13.77...
). This is relevant because there are no clear spatial correlations between the MRT of tropical C pools and mean annual temperature (MAT) or precipitation (MAP) ( Carvalhais et al., 2014Carvalhais N, Forkel M, Khomik M, Bellarby J, Jung M, Migliavacca M, Μu M, Saatchi S, Santoro M, Thurner M, Weber U, Ahrens B, Beer C, Cescatti A, Randerson JT, Reichstein M. Global covariation of carbon turnover times with climate in terrestrial ecosystems. Nature. 2014;514:213-7. https://doi.org/10.1038/nature13731
https://doi.org/10.1038/nature13731...
). Furthermore, since both MAT and evapotranspiration rates increase towards the Equator ( Huston and Wolverton, 2009Huston MA, Wolverton S. The global distribution of net primary production: resolving the paradox. Ecol Monogr. 2009;79:343-77. https://doi.org/10.1890/08-0588.1
https://doi.org/10.1890/08-0588.1...
), this aspect raises the question of the extent to which temperature and precipitation exert independent controls on tropical C pools.

Globally, vegetation and soil C pools show contrasting responses to temperature. Usually, both vegetation C pools and net primary productivity (NPP) increase with MAT at a rate varying between 5.0 and 13.0 Mg C ha–1 yr–1 °C–1, and this relationship is mirrored by a decrease in soil C pools at a rate of 8.0 Mg C ha–1 yr–1 °C–1 ( Raich et al., 2006Raich JW, Russell AE, Kitayama K, Parton WJ, Vitousek PM. Temperature influences carbon accumulation in moist tropical forests. Ecology. 2006;87:76-87. https://doi.org/10.1890/05-0023
https://doi.org/10.1890/05-0023...
). Consequently, it has been suggested that the increase in NPP with MAT is dependent on the positive correlation between MAT and soil respiration at global scales ( Raich and Schlesinger, 1992Raich JW, Schlesinger WH. The global carbon dioxide flux in soil respiration and its relationship to vegetation and climate. Tellus B. 1992;44:81-99. https://doi.org/10.3402/tellusb.v44i2.15428
https://doi.org/10.3402/tellusb.v44i2.15...
; Chapin et al., 2009Chapin FS, McFarland J, David McGuire A, Euskirchen ES, Ruess RW, Kielland K. The changing global carbon cycle: Linking plant-soil carbon dynamics to global consequences. J Ecol. 2009;97:840-50. https://doi.org/10.1111/j.1365-2745.2009.01529.x
https://doi.org/10.1111/j.1365-2745.2009...
). Despite the significance of these correlations, the processes and mechanisms underlying them remain poorly constrained. Moreover, because tropical regions are expected to undergo significant warming in the near future ( Almazroui et al., 2021Almazroui M, Ashfaq M, Islam MN, Rashid IU, Kamil S, Abid MA, O’Brien E, Ismail M, Reboita MS, Sörensson AA, Arias PA, Alves LM, Tippett MK, Saeed S, Haarsma R, Doblas-Reyes FJ, Saeed F, Kucharski F, Nadeem I, Silva-Vidal Y, Rivera JA, Ehsan MA, Martínez-Castro D, Muñoz ÁG, Ali MA, Coppola E, Sylla MB. Assessment of CMIP6 performance and projected temperature and precipitation changes over South America. Earth Syst Environ. 2021;5:155-83. https://doi.org/10.1007/s41748-021-00233-6
https://doi.org/10.1007/s41748-021-00233...
), the difference between MAP and evapotranspiration, i.e., ecosystem effective moisture ( Kramer and Chadwick, 2018Kramer MG, Chadwick OA. Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nat Clim Chang. 2018;8:1104-8. https://doi.org/10.1038/s41558-018-0341-4
https://doi.org/10.1038/s41558-018-0341-...
), may be significantly narrowed. Therefore, any rise in MAT should also bring consequences for the hydrological cycle.

Across the tropics, vegetation stores about 200–300 Pg C ( Mitchard, 2018Mitchard ETA. The tropical forest carbon cycle and climate change. Nature. 2018;559:527-34. https://doi.org/10.1038/s41586-018-0300-2
https://doi.org/10.1038/s41586-018-0300-...
) and soils hold about 630 Pg C within their first 1.00 m depth ( Jobbágy and Jackson, 2000Jobbágy E, Jackson R. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl. 2000;10:423-36. https://doi.org/10.1890/1051-0761(2000)010%255B0423:TVDOSO%255D2.0.CO%253B2
https://doi.org/10.1890/1051-0761(2000)0...
). In this case, both vegetation and soil C pools show positive correlations with MAP levels up to 3000 mm ( Schuur, 2003Schuur EAG. Productivity and global climate revisited: The sensitivity of tropical forest growth to precipitation. Ecology. 2003;84:1165-70. https://doi.org/10.1890/0012-9658(2003)084[1165:PAGCRT]2.0.CO;2
https://doi.org/10.1890/0012-9658(2003)0...
; Del Grosso et al., 2008Del Grosso S, Parton W, Stohlgren T, Zheng D, Bachelet D, Prince S, Hibbard K, Olson R. Global potential net primary production predicted from vegetation class, precipitation, and temperature. Ecology. 2008;89:2117-26. https://doi.org/10.1890/07-0850.1
https://doi.org/10.1890/07-0850.1...
). However, the control of moisture on soil C pools has long been considered indirect and dependent on the control of MAP levels on the vegetation ( Post et al., 1982Post WM, Emanuel WR, Zinke PJ, Stangenberger AG. Soil carbon pools and world life zones. Nature. 1982;298:156-9. https://doi.org/10.1038/298156a0
https://doi.org/10.1038/298156a0...
). Hence, MAP levels would primarily control NPP and vegetation C pools, which in turn, would determine C inputs into the soil and the size of its C pools. If so, vegetation and soil C pools should exhibit a strong spatial correlation. However, this view is contradicted by recent observations that high vegetation C pools are not necessarily spatially correlated with high soil C pools across the Brazilian territory ( Englund et al., 2017Englund O, Sparovek G, Berndes G, Freitas F, Ometto JP, Oliveira PVDCE, Costa C, Lapola D. A new high-resolution nationwide aboveground carbon map for Brazil. Geo Geogr Environ. 2017;4:e00045. https://doi.org/10.1002/geo2.45
https://doi.org/10.1002/geo2.45...
; Gomes et al., 2019Gomes LC, Faria RM, Souza E, Veloso GV, Schaefer CEGR, Fernades Filho EI. Modelling and mapping soil organic carbon stocks in Brazil. Geoderma. 2019;340:337-50. https://doi.org/10.1016/j.geoderma.2019.01.007
https://doi.org/10.1016/j.geoderma.2019....
). Moreover, in a study across 147 sites in humid forests across the Amazon, no clear relationships between soil C and climate (i.e., MAT and MAP) or aboveground biomass were found ( Quesada et al., 2020Quesada CA, Paz C, Mendoza EO, Phillips OL, Saiz G, Lloyd J. Variations in soil chemical and physical properties explain basin-wide Amazon forest soil carbon concentrations. Soil. 2020;6:53-88. https://doi.org/10.5194/soil-6-53-2020
https://doi.org/10.5194/soil-6-53-2020...
). Furthermore, correlations between soil C and MAP levels appear to depend on soil depth ( Jobbágy and Jackson, 2000Jobbágy E, Jackson R. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl. 2000;10:423-36. https://doi.org/10.1890/1051-0761(2000)010%255B0423:TVDOSO%255D2.0.CO%253B2
https://doi.org/10.1890/1051-0761(2000)0...
). These authors argue that the relative proportion of deep and shallow soil C pools is more dependent on plant C allocation than on climate itself. Overall, determining the extent to which vegetation and soil C pools respond independently to temperature, precipitation or ecosystem effective moisture is essential to predict the response of tropical C pools to environment changes, including rises in temperature and/or decreases in precipitation.

High temperatures and precipitation levels boost weathering rates and the development of deep soil profiles across the tropics ( Huston and Wolverton, 2009Huston MA, Wolverton S. The global distribution of net primary production: resolving the paradox. Ecol Monogr. 2009;79:343-77. https://doi.org/10.1890/08-0588.1
https://doi.org/10.1890/08-0588.1...
). Additionally, tropical soils are highly leached, with low availability of base cations and high capacity for P fixation ( Townsend et al., 2007Townsend AR, Cleveland CC, Asner GP, Bustamante MMC. Controls over foliar N:P ratios in tropical rain forests. Ecology. 2007;88:107-18. https://doi.org/10.1890/0012-9658(2007)88[107:COFNRI]2.0.CO;2
https://doi.org/10.1890/0012-9658(2007)8...
; Vitousek et al., 2010Vitousek PM, Porder S, Houlton BZ, Chadwick OA. Terrestrial phosphorus limitation: Mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl. 2010;20:5-15. https://doi.org/10.1890/08-0127.1
https://doi.org/10.1890/08-0127.1...
). Consequently, restricted nutrient availability may limit the responses of NPP to the “fertilization effect” of increasing levels of atmospheric CO2 ( Wieder et al., 2015Wieder WR, Cleveland CC, Smith WK, Todd-Brown K. Future productivity and carbon storage limited by terrestrial nutrient availability. Nat Geosci. 2015;8:441-4. https://doi.org/10.1038/ngeo2413
https://doi.org/10.1038/ngeo2413...
). Seemingly, the least limiting element required for plant growth in tropical ecosystems is N, which availability may be even in excess relative to other elements ( Martinelli et al., 1999Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K. Nitrogen stable isotopic composition of leaves and soil: Tropical versus temperate forests. Biogeochemistry. 1999;46:45-65. https://doi.org/10.1023/A:1006100128782
https://doi.org/10.1023/A:1006100128782...
; Hedin et al., 2009Hedin LO, Brookshire ENJ, Menge DNL, Barron AR. The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Evol Syst. 2009;40:613-35. https://doi.org/10.1146/annurev.ecolsys.37.091305.110246
https://doi.org/10.1146/annurev.ecolsys....
; Brookshire et al., 2012Brookshire ENJ, Gerber S, Menge DNL, Hedin LO. Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation. Ecol Lett. 2012;15:9-16. https://doi.org/10.1111/j.1461-0248.2011.01701.x
https://doi.org/10.1111/j.1461-0248.2011...
). The relative excess of N may be an important source of greenhouse gases such as nitrous oxide (N2O), which emissions appear to increase with decreasing P availability in humid ecosystems ( Hall and Matson, 1999Hall SJ, Matson PA. Nitrogen oxide emissions after nitrogen additions in tropical forests. Nature. 1999;400:152-5. https://doi.org/10.1038/22094
https://doi.org/10.1038/22094...
). However, it remains unknown whether nutrient availability can impact the response of vegetation and soil C pools to climate constraints ( Carvalhais et al., 2014Carvalhais N, Forkel M, Khomik M, Bellarby J, Jung M, Migliavacca M, Μu M, Saatchi S, Santoro M, Thurner M, Weber U, Ahrens B, Beer C, Cescatti A, Randerson JT, Reichstein M. Global covariation of carbon turnover times with climate in terrestrial ecosystems. Nature. 2014;514:213-7. https://doi.org/10.1038/nature13731
https://doi.org/10.1038/nature13731...
). Moreover, the extent to which the differential availability of P and N across the tropics exerts independent or joint controls on terrestrial C pools remains unclear.

Overall, the Brazilian territory provides a unique study area to analyze the feedbacks of tropical C pools to climate constraints. As such, Brazilian ecosystems are very diversified, including dry forests, semideciduous and humid forests, grasslands and mixed vegetation types ( Arruda et al., 2018Arruda DM, Schaefer CEGR, Fonseca RS, Solar RRC, Fernandes Filho EI. Vegetation cover of Brazil in the last 21 ka: New insights into the Amazonian refugia and Pleistocenic arc hypotheses. Glob Ecol Biogeogr. 2018;27:47-56. https://doi.org/10.1111/geb.12646
https://doi.org/10.1111/geb.12646...
). These ecosystems occur in an area spanning a latitude gradient between 5° N and 35° S and a longitude range between 35 and 75° W, where MAT varies between 10 and 26 °C and MAP levels can be less than 700 up to more than 3100 mm yr–1 ( Alvares et al., 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift. 2013;22:711-28. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
). Therefore, our overarching goal in this review is to rationalize the drivers of the horizontal distribution of vegetation and soil C pools as well as the vertical partitioning of C in the plant-soil continuum across the major Brazilian biomes.

MATERIALs AND METHODS

In this review, we searched the literature to investigate i) whether temperature and precipitation exert independent effects on C pools in Brazilian biomes; ii) the extent to which vegetation and soil C pools exhibit hierarchical feedbacks to climate, and iii) how these feedbacks are related to nutrient availability, especially P and N. To address the first question, we obtained data for MAP and MAT from the WorldClim Project, encompassing a temporal range from 1970 to 2000 ( Fick and Hijmans, 2017Fick SE, Hijmans RJ. WorldClim 2: new 1‐km spatial resolution climate surfaces for global land areas. Int J Climatol. 2017;37:4302-15. https://doi.org/10.1002/joc.5086
https://doi.org/10.1002/joc.5086...
). For evapotranspiration, the data obtained was based on the calibration of the MOD16 product for the period between 2000 and 2014 ( Dias et al., 2021Dias SHB, Filgueiras R, Fernandes Filho EI, Arcanjo GS, Silva GH, Mantovani EC, Cunha FF. Reference evapotranspiration of Brazil modeled with machine learning techniques and remote sensing. PLoS ONE. 2021;16:e0245834. https://doi.org/10.1371/journal.pone.0245834
https://doi.org/10.1371/journal.pone.024...
). Subsequently, we calculated the ecosystem effective moisture (EEM), that is, the difference between MAP and potential evapotranspiration ( Kramer and Chadwick, 2018Kramer MG, Chadwick OA. Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nat Clim Chang. 2018;8:1104-8. https://doi.org/10.1038/s41558-018-0341-4
https://doi.org/10.1038/s41558-018-0341-...
). According to these authors, the major weakness of this method is that the redistribution of water across the landscapes cannot be accurately accounted for in the calculation. Nonetheless, EEM should allow us to evaluate the interaction between precipitation and temperature in determining moisture availability considering the large area of the Brazilian territory. To address the second question, we combined the spatial distribution of vegetation ( Englund et al., 2017Englund O, Sparovek G, Berndes G, Freitas F, Ometto JP, Oliveira PVDCE, Costa C, Lapola D. A new high-resolution nationwide aboveground carbon map for Brazil. Geo Geogr Environ. 2017;4:e00045. https://doi.org/10.1002/geo2.45
https://doi.org/10.1002/geo2.45...
) and soil C pools ( Gomes et al., 2019Gomes LC, Faria RM, Souza E, Veloso GV, Schaefer CEGR, Fernades Filho EI. Modelling and mapping soil organic carbon stocks in Brazil. Geoderma. 2019;340:337-50. https://doi.org/10.1016/j.geoderma.2019.01.007
https://doi.org/10.1016/j.geoderma.2019....
) across the Brazilian territory with 1 km spatial resolution. Our maps and figures were plotted using the R software. Aboveground vegetation C pools included an up-to-date land use/cover determined in 2016 with a spatial resolution of 50 m as part of the communication to the United Nations Framework Convention on Climate Change (UNFCCC) ( Englund et al., 2017Englund O, Sparovek G, Berndes G, Freitas F, Ometto JP, Oliveira PVDCE, Costa C, Lapola D. A new high-resolution nationwide aboveground carbon map for Brazil. Geo Geogr Environ. 2017;4:e00045. https://doi.org/10.1002/geo2.45
https://doi.org/10.1002/geo2.45...
). Soil C pools were based on a data set that included 8,227 soil profiles and the analysis of 37,693 samples. This soil survey and sampling was conducted by the RADAM Project in the period between 1973 and 1986 ( Gomes et al., 2019Gomes LC, Faria RM, Souza E, Veloso GV, Schaefer CEGR, Fernades Filho EI. Modelling and mapping soil organic carbon stocks in Brazil. Geoderma. 2019;340:337-50. https://doi.org/10.1016/j.geoderma.2019.01.007
https://doi.org/10.1016/j.geoderma.2019....
). For this reason, we could not restrict our discussion to natural ecosystems and patterns associated to land-use change had to be considered to some extent. Although the data for vegetation and soil C pools were not obtained in the same timeframe, it is expected that latter is much less sensitive to land-use change than the former ( Boy et al., 2018Boy J, Strey S, Schönenberg R, Strey R, Weber-Santos O, Nendel C, Klingler M, Schumann C, Hartberger K, Guggenberger G. Seeing the forest not for the carbon: why concentrating on land-use-induced carbon stock changes of soils in Brazil can be climate-unfriendly. Reg Environ Chang. 2018;18:63-75. https://doi.org/10.1007/s10113-016-1008-1
https://doi.org/10.1007/s10113-016-1008-...
). Based on the data obtained for MAT, MAP, EEM, vegetation and soil C pools, we obtained Pearson’s correlation coefficients among these variables for each biome (Amazon, Caatinga, Cerrado, Atlantic Forest, Pampa, and Pantanal) as shown in table 1 .

Table 1
Pearson’s correlation coefficients ( r ) for the spatial distribution of mean annual precipitation (MAP), temperature (MAT), ecosystem effective moisture (EEM), plant and soil C pools across the six Brazilian biomes and the whole country

We addressed the third question by searching the literature for studies evaluating i) nutrient resorption preceding leaf senescence, ii) nutrient mineralization in plant litter and soil organic matter, and iii) plant responses to seasonal variations in moisture availability. This step allowed us to infer a relationship between nutrient dynamics as constrained by climate, the horizontal distribution and vertical partition of C in plant-soil systems. A synthesis of the information gathered in those studies is given in table 2 and was used to support a conceptual framework to link climate constraints and terrestrial C pools in Brazil. Not all studies included in this analysis were conducted in Brazilian biomes, but we tried to be as specific as possible.

Table 2
Major climate constraints (temperature and precipitation) on ecosystem effective moisture (EEM) and their impacts on ecosystem C pools (vegetation and soils) across the major Brazilian biomes and supporting evidence from the literature consulted

RESULTS AND DISCUSSION

Temperature and precipitation across the Brazilian territory

Across the Amazon, most of its ecosystems occur in areas where MAT is above 22 °C and MAP levels are predominantly higher than 1800 mm ( Figure 1 ). According to the Köppen classification system, the most common climate classes in these areas are Af and Am ( Alvares et al., 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift. 2013;22:711-28. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
). In sharp contrast with the Amazon, the Caatinga domain is marked by high MAT (above 22–24 °C) overlapping with very low MAP levels, usually varying between 700 and 1000 mm yr-1 ( Figure 1 ). In this biome, As and Bs climates predominate ( Alvares et al., 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift. 2013;22:711-28. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
). Hence, the Amazon and the Caatinga represent the sharpest contrast in MAP levels in Brazil.

Figure 1
Distribution of frequency for mean annual precipitation (MAP) and mean annual temperature (MAT) across the six major Brazilian biomes, namely Amazon, Caatinga, Cerrado, Atlantic Forest, Pampa and Pantanal.

Across the Cerrado, MAT is consistently higher than 22 °C, while MAP levels vary between 1000 and 1900 mm yr–1. This upper limit in MAP levels marks the northwest border between the Cerrado and the Amazon domain ( Figure 1 ). Although precipitation levels are relatively high in the Cerrado, rainfall has a strong seasonality, with humid and dry seasons lasting approximately six months each. In the northeast, deciduous forests mark the border between the Cerrado and the Caatinga ( Arruda et al., 2018Arruda DM, Schaefer CEGR, Fonseca RS, Solar RRC, Fernandes Filho EI. Vegetation cover of Brazil in the last 21 ka: New insights into the Amazonian refugia and Pleistocenic arc hypotheses. Glob Ecol Biogeogr. 2018;27:47-56. https://doi.org/10.1111/geb.12646
https://doi.org/10.1111/geb.12646...
). At the southwest border of the Cerrado occurs the Pantanal biome, which is marked by high MAT (mostly 24–27 °C) and MAP levels varying between 1000–1500 mm yr–1 ( Figure 1 ). Typically, the predominant climate class in the Cerrado are Aw and Am, whereas, both Aw and Af can occur across the Pantanal ( Alvares et al., 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift. 2013;22:711-28. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
).

Generally, the Atlantic Forest shows the widest MAT range (15–25 °C) relative to the other Brazilian biomes ( Figure 2 ). In this biome, deciduous, semideciduous, and mixed forests predominate ( Arruda et al., 2018Arruda DM, Schaefer CEGR, Fonseca RS, Solar RRC, Fernandes Filho EI. Vegetation cover of Brazil in the last 21 ka: New insights into the Amazonian refugia and Pleistocenic arc hypotheses. Glob Ecol Biogeogr. 2018;27:47-56. https://doi.org/10.1111/geb.12646
https://doi.org/10.1111/geb.12646...
). In the SE-NE transect across the Atlantic Forest domain, deciduous forests determine a border with the Caatinga, coinciding with reduced EEM levels ( Figure 2 ). Similar levels of EEM also occur at the southwest border between the Atlantic Forest and the Cerrado, but semideciduous forests predominate ( Arruda et al., 2018Arruda DM, Schaefer CEGR, Fonseca RS, Solar RRC, Fernandes Filho EI. Vegetation cover of Brazil in the last 21 ka: New insights into the Amazonian refugia and Pleistocenic arc hypotheses. Glob Ecol Biogeogr. 2018;27:47-56. https://doi.org/10.1111/geb.12646
https://doi.org/10.1111/geb.12646...
). At latitudes higher than 20° S, both the Atlantic Forest and the Pampa occur in areas where MAT is consistently below 25 °C, with MAP varying between 1000 and 1900 mm yr–1 ( Figure 1 ). Across the Atlantic Forest domain, MAT showed a relatively strong negative correlation with both MAP and EEM levels ( Table 1 ). Mixed forests mark the southern border between the Atlantic Forest and the Pampa ( Arruda et al., 2018Arruda DM, Schaefer CEGR, Fonseca RS, Solar RRC, Fernandes Filho EI. Vegetation cover of Brazil in the last 21 ka: New insights into the Amazonian refugia and Pleistocenic arc hypotheses. Glob Ecol Biogeogr. 2018;27:47-56. https://doi.org/10.1111/geb.12646
https://doi.org/10.1111/geb.12646...
). In contrast to the Atlantic Forest, the Pampa domain is marked by a narrow temperature range (17–20 °C), as shown in figure 1 . For the Atlantic Forest, the predominant climate classes are Cwa, Cwb, Cfa and Cfb, whereas Cfa predominates across the Pampa ( Alvares et al., 2013Alvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift. 2013;22:711-28. https://doi.org/10.1127/0941-2948/2013/0507
https://doi.org/10.1127/0941-2948/2013/0...
). Overall, there is a substantial overlap in MAP levels for the Cerrado, Pantanal, Atlantic Forest, and the Pampa in the range between 1000 and 1800 mm yr–1 ( Figure 1 ).

Figure 2
Spatial distribution of annual and seasonal ecosystem effective moisture (EEM), i.e., the difference between mean annual precipitation and potential evapotranspiration ( Kramer and Chadwick, 2018Kramer MG, Chadwick OA. Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nat Clim Chang. 2018;8:1104-8. https://doi.org/10.1038/s41558-018-0341-4
https://doi.org/10.1038/s41558-018-0341-...
) across the Brazilian territory. Summer: December–February; Autumn: March–May; Winter: June–August; and Spring: September–November.

Ecosystem effective moisture: the interaction between temperature and precipitation

For most of the area under the Amazon domain, the relatively well distributed annual volume of precipitation is translated into EEM levels predominantly positive (>630 mm yr–1) ( Figure 2 ). Although high temperatures favor high evapotranspiration rates, EEM showed the strongest spatial correlation with MAP ( r = 0.99) across the Amazon ( Table 1 ). Otherwise, high temperatures and low precipitation rates combined led to EEM levels varying between –650 and –1250 mm yr–1 across the Caatinga ( Figure 2 ).

Across the Cerrado, EEM levels can vary between negative (–280 mm yr–1) and positive values (+330 mm yr–1) as shown figure 2 . The overall variability in EEM levels for the Cerrado is consistent with its geographic distribution in central Brazil, bordering with the Amazon in northwest, the Caatinga in northeast, the Atlantic Forest in southeast, and the Pantanal to the west ( Figure 2 ). Across the Pantanal domain, EEM levels are predominantly negative (0 to –1000 mm yr–1), which is likely an underestimation because many ecosystems occurring in this biome are wetlands located in depressional areas. Hence, the redistribution of water within landscapes cannot be well represented in the EEM estimates ( Kramer and Chadwick, 2018Kramer MG, Chadwick OA. Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nat Clim Chang. 2018;8:1104-8. https://doi.org/10.1038/s41558-018-0341-4
https://doi.org/10.1038/s41558-018-0341-...
).

Atlantic Forest and the Pampa show similar EEM levels at latitudes higher than approximately 20° S, as shown in figure 2 . Given the overall wide range in temperature observed for the Atlantic Forest ( Figure 1 ) and its reduced precipitation levels during the winter, EEM levels in this area can vary between –1000 up to 500 mm yr–1 ( Figure 2 ). Geographically, the negative levels of EEM occur predominantly across a SW-NE transect bordering with the Cerrado and the Caatinga in the northeast ( Figure 2 ). The exception in this case is a narrow strip of land located along the coast of the Atlantic Ocean. Across the Pampa, where precipitation levels are usually reduced during the summer, annual EEM is predominantly positive (0 to 500 mm yr–1). Several lines of evidence indicate that the predominant native vegetation of the Pampa, that is, Campos das Missões or Campos de Barba-de-Bode ( Aristida jubata ), reflects past climates conditions that were dryer than the current climate ( Behling et al., 2009Behling H, Jeske-Pieruschka V, Schüler L, Pillar VDP. Dinâmica dos campos no sul do Brasil durante o Quaternário Tardio. In: Pillar VDP, Müller SC, Castilhos ZMS, Jacques AVA, editors. Campos sulinos: conservação e uso sustentável da biodiversidade. Brasília, DF: MMA; 2009. p. 13-25. ; Verdum et al., 2019Verdum R, Vieira LFS, Caneppele JCG, Gass SLB. Pampa: The south Brazil. In: Salgado AAR, Santos LJC, Paisani JC, editors. The physical geography of Brazil. Geography of the physical environment. Cham: Springer International Publishing; 2019. p. 7-20. https://doi.org/10.1007/978-3-030-04333-9_2
https://doi.org/10.1007/978-3-030-04333-...
).

As expected, EEM showed stronger spatial correlation with MAP than with MAT in all biomes considered ( Table 1 ). Overall, the Atlantic Forest domain stands out as the biome where MAT and EEM showed the strongest negative correlation ( r = –0.70) ( Table 1 ).

Under high MAT-EEM constraints, nutrient dynamics determine the relative C sink strength of vegetation and soil

Because many elements can limit NPP in tropical regions ( Townsend et al., 2011Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC. Multi-element regulation of the tropical forest carbon cycle. Front Ecol Environ. 2011;9:9-17. https://doi.org/10.1890/100047
https://doi.org/10.1890/100047...
), plants growing in humid ecosystems appear to invest proportionally more C in organs with long timespan to increase their nutrient use efficiency ( Herrera et al., 1978Herrera R, Merida T, Stark N, Jordan CF. Direct phosphorus transfer from leaf litter to roots. Naturwissenschaften. 1978;65:208-9. https://doi.org/10.1007/BF00450594
https://doi.org/10.1007/BF00450594...
; Aerts, 1995Aerts R. The advantages of being evergreen. Trends Ecol Evol. 1995;10:402-7. https://doi.org/10.1016/S0169-5347(00)89156-9
https://doi.org/10.1016/S0169-5347(00)89...
; Wardle et al., 2004Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten WH, Wall DH. Ecological linkages between aboveground and belowground biota. Science. 2004;304:1629-33. https://doi.org/10.1126/science.1094875
https://doi.org/10.1126/science.1094875...
; Körner, 2017Körner C. A matter of tree longevity. Science. 2017;355:130-1. https://doi.org/10.1126/science.aal2449
https://doi.org/10.1126/science.aal2449...
). Further, high resorption rates of nutrients often precede leaf senescence ( Vergütz et al., 2012Vergütz L, Manzoni S, Porporato A, Novais RF, Jackson RB. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr. 2012;82:205-20. https://doi.org/10.1890/11-0416.1
https://doi.org/10.1890/11-0416.1...
), whereas some nutrients are recycled during the breakdown of plant litter in the soils. These traits can have at least three major consequences for terrestrial C dynamics in humid ecosystems under high MAT coupled to high MAP controlling EEM levels.

Firstly, owing to the high resorption of nutrients, especially P ( Vitousek and Sanford, 1986Vitousek PM, Sanford RL. Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst. 1986;17:137-67. https://doi.org/10.1146/annurev.es.17.110186.001033
https://doi.org/10.1146/annurev.es.17.11...
), tropical plants growing in humid ecosystems produce litter showing wide C:P and/or N:P ratios ( Cleveland and Liptzin, 2007Cleveland CC, Liptzin D. C:N:P stoichiometry in soil: Is there a “Redfield ratio” for the microbial biomass? Biogeochemistry. 2007;85:235-52. https://doi.org/10.1007/s10533-007-9132-0
https://doi.org/10.1007/s10533-007-9132-...
). These wide elemental relations have a negative impact on the C use efficiency of soil decomposers ( Cleveland et al., 2002Cleveland CC, Townsend AR, Schmidt SK. Phosphorus limitation of microbial processes in moist tropical forests: Evidence from short-term laboratory incubations and field studies. Ecosystems. 2002;5:680-91. https://doi.org/10.1007/s10021-002-0202-9
https://doi.org/10.1007/s10021-002-0202-...
; Camenzind et al., 2018Camenzind T, Hättenschwiler S, Treseder KK, Lehmann A, Rillig MC. Nutrient limitation of soil microbial processes in tropical forests. Ecol Monogr. 2018;88:4-21. https://doi.org/10.1002/ecm.1279
https://doi.org/10.1002/ecm.1279...
). Generally, it is well known that microbes growing on substrates with wide C-to-nutrients ratios exhibit low C use efficiency due to stoichiometric constraints ( Manzoni et al., 2010Manzoni S, Trofymow JA, Jackson RB, Porporato A. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr. 2010;80:89-106. https://doi.org/10.1890/09-0179.1
https://doi.org/10.1890/09-0179.1...
; Zechmeister-Boltenstern et al., 2015Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J, Wanek W. The application of ecological stoichiometry to plant-microbial-soil organic matter transformations. Ecol Monogr. 2015;85:133-55. https://doi.org/10.1890/14-0777.1
https://doi.org/10.1890/14-0777.1...
). This means that a given microbial community attempts to narrow C-to-nutrients ratios by eliminating the relative “excess” of C in the substrate. Alternatively, stoichiometric constraints can be minimized by means of succession among distinct microbial communities in soil food webs ( Kaiser et al., 2014Kaiser C, Franklin O, Dieckmann U, Richter A. Microbial community dynamics alleviate stoichiometric constraints during litter decay. Ecol Lett. 2014;17:680-90. https://doi.org/10.1111/ele.12269
https://doi.org/10.1111/ele.12269...
; Maynard et al., 2017Maynard DS, Crowther TW, Bradford MA. Fungal interactions reduce carbon use efficiency. Ecol Lett. 2017;20:1034-42. https://doi.org/10.1111/ele.12801
https://doi.org/10.1111/ele.12801...
). In this case, different microbial communities drive substrate breakdown as the C-to-nutrients ratio narrows down. Hence, whether a single microbial community attempts to narrow C-to-nutrients ratios via increased respiration or engage in microbial succession, proportionally more C should be lost as CO2. Moreover, soil microbes should use C less efficiently under high temperatures ( Manzoni et al., 2012Manzoni S, Taylor P, Richter A, Porporato A, Ågren GI. Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol. 2012;196:79-91. https://doi.org/10.1111/j.1469-8137.2012.04225.x
https://doi.org/10.1111/j.1469-8137.2012...
; Frey et al., 2013Frey SD, Lee J, Melillo JM, Six J. The temperature response of soil microbial efficiency and its feedback to climate. Nat Clim Chang. 2013;3:395-8. https://doi.org/10.1038/nclimate1796
https://doi.org/10.1038/nclimate1796...
; Qiao et al., 2019Qiao Y, Wang J, Liang G, Du Z, Zhou J, Zhu C, Huang K, Zhou X, Luo Y, Yan L, Xia J. Global variation of soil microbial carbon-use efficiency in relation to growth temperature and substrate supply. Sci Rep. 2019;9:5621. https://doi.org/10.1038/s41598-019-42145-6
https://doi.org/10.1038/s41598-019-42145...
). Therefore, under these environmental and biological constraints, the contribution of microbial-derived products to form soil C pools should be significantly reduced ( Cotrufo et al., 2013Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E. The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol. 2013;19:988-95. https://doi.org/10.1111/gcb.12113
https://doi.org/10.1111/gcb.12113...
).

The second aspect concerning nutrient cycling is that a relative excess of N in humid ecosystems may help to keep fast mineralization rates of plant litter. The most recurrent evidence supporting this inference is that humid tropical ecosystems are marked by significant losses of gaseous N, especially via denitrification ( Martinelli et al., 1999Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K. Nitrogen stable isotopic composition of leaves and soil: Tropical versus temperate forests. Biogeochemistry. 1999;46:45-65. https://doi.org/10.1023/A:1006100128782
https://doi.org/10.1023/A:1006100128782...
; Breuer et al., 2002Breuer L, Kiese R, Butterbach-Bahl K. Temperature and moisture effects on nitrification rates in tropical rain-forest soils. Soil Sci Soc Am J. 2002;66:834-44. https://doi.org/10.2136/sssaj2002.8340
https://doi.org/10.2136/sssaj2002.8340...
; Davidson et al., 2007Davidson EA, Carvalho CJR, Figueira AM, Ishida FY, Ometto JPHB, Nardoto GB, Sabá RT, Hayashi SN, Leal EC, Vieira ICG, Martinelli LA. Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature. 2007;447:995-8. https://doi.org/10.1038/nature05900
https://doi.org/10.1038/nature05900...
). These losses characterize an “open N cycle” in many tropical humid forests ( Martinelli et al., 1999Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K. Nitrogen stable isotopic composition of leaves and soil: Tropical versus temperate forests. Biogeochemistry. 1999;46:45-65. https://doi.org/10.1023/A:1006100128782
https://doi.org/10.1023/A:1006100128782...
). We interpret such “openness” in the N cycle as a mechanism to keep high rates of litter mineralization in ecosystems where soil water content is frequently above field capacity or high enough to saturate the soil pore space ( Bollmann and Conrad, 1998Bollmann A, Conrad R. Influence of O2availability on NO and N2O release by nitrification and denitrification in soils. Glob Chang Biol. 1998;4:387-96. https://doi.org/10.1046/j.1365-2486.1998.00161.x
https://doi.org/10.1046/j.1365-2486.1998...
). In such circumstances, nitrate can be used as an alternative electron acceptor when the levels of oxygen drop significantly and aerobic respiration cannot proceed normally, especially within soil aggregates ( Houlton et al., 2006Houlton BZ, Sigman DM, Hedin LO. Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci. 2006;103:8745-50. https://doi.org/10.1073/pnas.0510185103
https://doi.org/10.1073/pnas.0510185103...
; Butterbach-Bahl et al., 2013Butterbach-Bahl K, Baggs EM, Dannenmann M, Kiese R, Zechmeister-Boltenstern S. Nitrous oxide emissions from soils: how well do we understand the processes and their controls? Phil Trans R Soc B. 2013;368:20130122. https://doi.org/10.1098/rstb.2013.0122
https://doi.org/10.1098/rstb.2013.0122...
; Keiluweit et al., 2016Keiluweit M, Nico PS, Kleber M, Fendorf S. Are oxygen limitations under recognized regulators of organic carbon turnover in upland soils? Biogeochemistry. 2016;127:157-71. https://doi.org/10.1007/s10533-015-0180-6
https://doi.org/10.1007/s10533-015-0180-...
). This reasoning is also consistent with increases in denitrification rates with decreasing P availability ( Hall and Matson, 1999Hall SJ, Matson PA. Nitrogen oxide emissions after nitrogen additions in tropical forests. Nature. 1999;400:152-5. https://doi.org/10.1038/22094
https://doi.org/10.1038/22094...
). Thus, denitrification would allow high mineralization rates of plant litter, soil organic matter to favor fast P cycling that sustain high vegetation C pools in ecosystems under high EEM ( Figure 3 ).

Figure 3
Spatial distribution of vegetation and soil C pools, and their sum to yield the ecosystem C pool in Brazil. The spatial distribution of vegetation C pools has been published by Englund et al. (2017)Englund O, Sparovek G, Berndes G, Freitas F, Ometto JP, Oliveira PVDCE, Costa C, Lapola D. A new high-resolution nationwide aboveground carbon map for Brazil. Geo Geogr Environ. 2017;4:e00045. https://doi.org/10.1002/geo2.45
https://doi.org/10.1002/geo2.45...
. Soil C pools included observations from more than 8,200 soil profiles as described elsewhere by Gomes et al. (2019)Gomes LC, Faria RM, Souza E, Veloso GV, Schaefer CEGR, Fernades Filho EI. Modelling and mapping soil organic carbon stocks in Brazil. Geoderma. 2019;340:337-50. https://doi.org/10.1016/j.geoderma.2019.01.007
https://doi.org/10.1016/j.geoderma.2019....
.

A third important aspect is that many plants in humid ecosystems have shallow root mats to optimize nutrient recycling from decaying plant litter ( Stark and Jordan, 1978Stark NM, Jordan CF. Nutrient retention by the root mat of an Amazonian rain forest. Ecology. 1978;59:434-7. https://doi.org/10.2307/1936571
https://doi.org/10.2307/1936571...
; Jordan and Escalante, 1980Jordan CF, Escalante G. Root productivity in an amazonian rain forest. Ecology. 1980;61:14-8. https://doi.org/10.2307/1937148
https://doi.org/10.2307/1937148...
; Kingsbury and Kellman, 1997Kingsbury N, Kellman M. Root mat depths and surface soil chemistry in Southeastern Venezuela. J Trop Ecol. 1997;13:475-9. https://doi.org/10.1017/S0266467400010646
https://doi.org/10.1017/S026646740001064...
). Critically, shallow root mats are not restricted to low fertility soils across the tropics ( Sayer et al., 2006Sayer EJ, Tanner EVJ, Cheesman AW. Increased litterfall changes fine root distribution in a moist tropical forest. Plant Soil. 2006;281:5-13. https://doi.org/10.1007/s11104-005-6334-x
https://doi.org/10.1007/s11104-005-6334-...
), suggesting that high MAP-EEM is essential for this trait to be effective ( Figure 2 ). As the plant material decomposes on the soil surface, a shallow and thick root mat also would help to reduce P fixation in the oxidic soils underneath tropical forests ( Herrera et al., 1978Herrera R, Merida T, Stark N, Jordan CF. Direct phosphorus transfer from leaf litter to roots. Naturwissenschaften. 1978;65:208-9. https://doi.org/10.1007/BF00450594
https://doi.org/10.1007/BF00450594...
). However, because the roots are concentrated on the soil surface, their contact with soil minerals is reduced, and so should be their contribution to soil C pools ( Lavallee et al., 2018Lavallee JM, Conant RT, Paul EA, Cotrufo MF. Incorporation of shoot versus root-derived13C and15N into mineral-associated organic matter fractions: results of a soil slurry incubation with dual-labelled plant material. Biogeochemistry. 2018;137:379-93. https://doi.org/10.1007/s10533-018-0428-z
https://doi.org/10.1007/s10533-018-0428-...
). Hence, with increasing MAP and EEM levels, proportionally more soil C is stored within the first 0.30 m of topsoil ( Moraes et al., 1995Moraes JL, Cerri CC, Melillo JM, Kicklighter D, Neill C, Steudler PA, Skole DL. Soil carbon stocks of the Brazilian Amazon Basin. Soil Sci Soc Am J. 1995;59:244-7. https://doi.org/10.2136/sssaj1995.03615995005900010038x
https://doi.org/10.2136/sssaj1995.036159...
; Jobbágy and Jackson, 2000Jobbágy E, Jackson R. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl. 2000;10:423-36. https://doi.org/10.1890/1051-0761(2000)010%255B0423:TVDOSO%255D2.0.CO%253B2
https://doi.org/10.1890/1051-0761(2000)0...
). This also may help to explain why the correlations between soil C pools and MAP tend to decrease with soil depth ( Jobbágy and Jackson, 2000Jobbágy E, Jackson R. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl. 2000;10:423-36. https://doi.org/10.1890/1051-0761(2000)010%255B0423:TVDOSO%255D2.0.CO%253B2
https://doi.org/10.1890/1051-0761(2000)0...
). Otherwise, the retention of soil C in mineral-organic associations at depths below 0.30 m should depend proportionally more on water transport than on deep rooting ( Kalbitz et al., 2000Kalbitz K, Solinger S, Park JH, Michalzik B, Matzner E. Controls on the dynamics of dissolved organic matter in soils: A review. Soil Sci. 2000;165:277-304. https://doi.org/10.1097/00010694-200004000-00001
https://doi.org/10.1097/00010694-2000040...
; Schwendenmann and Veldkamp, 2005Schwendenmann L, Veldkamp E. The role of dissolved organic carbon, dissolved organic nitrogen, and dissolved inorganic nitrogen in a tropical wet forest ecosystem. Ecosystems. 2005;8:339-51. https://doi.org/10.1007/s10021-003-0088-1
https://doi.org/10.1007/s10021-003-0088-...
; Kramer and Chadwick, 2018Kramer MG, Chadwick OA. Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nat Clim Chang. 2018;8:1104-8. https://doi.org/10.1038/s41558-018-0341-4
https://doi.org/10.1038/s41558-018-0341-...
). All these factors contribute to weaken the soil C sink strength in humid ecosystems, while favoring the vegetation C pool ( Figure 3 ). As such, across the Amazon domain, soil C pools vary in the range between 7.5 to 10 kg m–2, whereas vegetation C pools can be as high 27 kg m–2 ( Figure 3 ). Our study highlights that vegetation C pools showed the strongest spatial correlation with both MAP and EEM across the Amazon domain compared to the other Brazilian biomes ( Table 1 ).

Our analysis indicates a potential mechanistic connection to explain the correlation between soil respiration and NPP in moist tropical ecosystems ( Raich and Potter, 1995Raich JW, Potter CS. Global patterns of carbon dioxide emissions from soils. Global Biogeochem Cycles. 1995;9:23-36. https://doi.org/10.1029/94GB02723
https://doi.org/10.1029/94GB02723...
; Chapin et al., 2009Chapin FS, McFarland J, David McGuire A, Euskirchen ES, Ruess RW, Kielland K. The changing global carbon cycle: Linking plant-soil carbon dynamics to global consequences. J Ecol. 2009;97:840-50. https://doi.org/10.1111/j.1365-2745.2009.01529.x
https://doi.org/10.1111/j.1365-2745.2009...
). Further, the dependence of a strong vegetation C pool on a weakened soil C sink strength under high EEM contributes to explain the lack of correlations between the MRT of tropical C pools and MAT or MAP as isolate variables ( Carvalhais et al., 2014Carvalhais N, Forkel M, Khomik M, Bellarby J, Jung M, Migliavacca M, Μu M, Saatchi S, Santoro M, Thurner M, Weber U, Ahrens B, Beer C, Cescatti A, Randerson JT, Reichstein M. Global covariation of carbon turnover times with climate in terrestrial ecosystems. Nature. 2014;514:213-7. https://doi.org/10.1038/nature13731
https://doi.org/10.1038/nature13731...
). It is important to point out that these correlations may be low because vegetation and soil C combined may overestimate the MRT of the latter pool, and this aspect warrants further research. Hence, it seems reasonable that only in areas where high temperatures cannot override the control of precipitation on EEM, high throughput rates of C and water maximize both vegetation and ecosystem C pools ( Figure 4 ; Table 1 ). However, this feature comes at ‘a price’ of a weak soil C sink. Thus, vegetation and soil C pools in humid ecosystems show opposite, but essentially hierarchical responses to climate. Therefore, the overall high turnover rates of litter and soil organic matter are ultimately the driver of high ecosystem C pools dominated by the vegetation.

Figure 4
Conceptual model to describe the control of temperature and precipitation on ecosystem effective moisture (EEM), which in turn determines the partition of C and vegetation and soils across the six major Brazilian biomes: Amazon, Cerrado, Pantanal, Caatinga, Pampa and Atlantic Forest.

Temperature as a key factor for EEM with increasing seasonality of precipitation

Across the Brazilian territory, temperature appears to exert an increasing control on EEM as the seasonality of precipitation increases. However, the strongest negative correlation between MAT and EEM was observed for the Atlantic Forest ( Table 1 ), probably owing to its wider temperature range as compared to the other biomes ( Figure 1 ). Nonetheless, two major subregions can be identified: one region includes areas where temperatures remain elevated as precipitation rates decrease, and another region where both temperatures and precipitation decrease approximately simultaneously.

Decreasing precipitation under constantly high temperatures

In areas under persistently high temperatures and seasonal precipitation, the reduction in EEM is critical for C cycling in large areas of the Cerrado and the Caatinga ( Figure 2 ). In some areas of the Caatinga, water limitation is so severe that it can even restrict weathering and pedogenesis, and consequently, soil C pools can be constrained by shallow soil profiles ( Corrêa et al., 2019Corrêa ACB, Tavares BAC, Lira DR, Mutzenberg DS, Cavalcanti LCS. The semi-arid domain of the Northeast of Brazil. In: Salgado AAR, Santos LJC, Paisani JC, editors. The physical geography of Brazil. Geography of the physical environment. Cham: Springer International Publishing; 2019. p. 119-50. https://doi.org/10.1007/978-3-030-04333-9_7
https://doi.org/10.1007/978-3-030-04333-...
). Hence, because MAP levels limit the leaching of soil nutrients, their availability to plants in ecosystems across the Caatinga can be sufficient during the short humid season ( Figure 2 ). Owing to the overall low MAP, high MAT and the resulting low EEM observed across the Caatinga domain, NPP is so low that it may limit C inputs into the soils ( Dexter et al., 2018Dexter KG, Pennington RT, Oliveira-Filho AT, Bueno ML, Miranda PLS, Neves DM. Inserting tropical dry forests into the discussion on biome transitions in the tropics. Front Ecol Evol. 2018;6:104. https://doi.org/10.3389/fevo.2018.00104
https://doi.org/10.3389/fevo.2018.00104...
). Thus, both vegetation and soil C pools are low ( Figure 3 ) and they show unidirectional responses to climate.

For ecosystems occurring across the Cerrado domain, periods of high precipitation and EEM levels are intercalated by equally long dry seasons ( Figure 2 ). Therefore, high temperatures can favor C fixation during the humid season, despite the widespread occurrence of low fertility soils ( Coutinho, 1990Coutinho LM. Fire in the ecology of the Brazilian Cerrado. In: Goldammer JG, editor. Fire in the Tropical Biota. Ecological Studies (Analysis and Synthesis). Heidelberg: Springer; 1990. p. 82-105. ; Sarmiento, 1992Sarmiento G. Adaptive strategies of perennial grasses in South American savannas. J Veg Sci. 1992;3:325-36. https://doi.org/10.2307/3235757
https://doi.org/10.2307/3235757...
). Subsequently, decreases in precipitation coupled to persistently high temperatures cause EEM levels to drop significantly and part of the living vegetation may dry out ( Moritz et al., 2005Moritz MA, Morais ME, Summerell LA, Carlson JM, Doyle J. Wildfires, complexity, and highly optimized tolerance. Proc Natl Acad Sci. 2005;102:17912-7. https://doi.org/10.1073/pnas.0508985102
https://doi.org/10.1073/pnas.0508985102...
). Dried plant material becomes flammable and can fuel wildfires ( Bond and Keeley, 2005Bond WJ, Keeley JE. Fire as a global “herbivore”: The ecology and evolution of flammable ecosystems. Trends Ecol Evol. 2005;20:387-94. https://doi.org/10.1016/j.tree.2005.04.025
https://doi.org/10.1016/j.tree.2005.04.0...
), leading to significant loss of nutrients by volatilization, particularly N and S ( Pivello and Coutinho, 1992Pivello VR, Coutinho LM. Transfer of macro-nutrients to the atmosphere during experimental burnings in an open cerrado (Brazilian savanna). J Trop Ecol. 1992;8:487-7. https://doi.org/10.1017/S0266467400006829
https://doi.org/10.1017/S026646740000682...
). Other elements such as K, Ca, and Mg are usually concentrated in the ashes on the soil surface ( Coutinho, 1990Coutinho LM. Fire in the ecology of the Brazilian Cerrado. In: Goldammer JG, editor. Fire in the Tropical Biota. Ecological Studies (Analysis and Synthesis). Heidelberg: Springer; 1990. p. 82-105. ), and these elements can be transported by wind during the dry season or by runoff in the subsequent humid season. In long-term, the impact of fire on soil fertility could be a deterrent to the size of vegetation C pools in such ecosystems ( Figure 3 ). According to a survey across 70 sites in the Cerrado, total biomass production varied from 24 Mg ha–1 in grasslands up to 98 Mg ha–1 in forestlands ( Miranda et al., 2014Miranda SC, Bustamante M, Palace M, Hagen S, Keller M, Ferreira LG. Regional variations in biomass distribution in Brazilian savanna woodland. Biotropica. 2014;46:125-38. https://doi.org/10.1111/btp.12095
https://doi.org/10.1111/btp.12095...
). These values would represent only a small fraction of the plant biomass observed across the Amazon under similar temperatures ( Figure 3 ). Seemingly, Cerrado trees allocate a significant amount of C in organs such as thick barks to withstand fire ( Simon and Pennington, 2012Simon MF, Pennington T. Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian Cerrado. Int J Plant Sci. 2012;173:711-23. https://doi.org/10.1086/665973
https://doi.org/10.1086/665973...
), but these adaptations ultimately may contribute to reduce their overall NPP.

Although fire events can quickly convert more than 80 % of the plant litter into CO2 ( Kauffman et al., 1994Kauffman JB, Cummings DL, Ward DE. Relationships of fire, biomass and nutrient dynamics along a vegetation gradient in the Brazilian Cerrado. J Ecol. 1994;82:519-31. https://doi.org/10.2307/2261261
https://doi.org/10.2307/2261261...
), pyrogenic carbonaceous materials can be added to the soil C pool. However, there is limited information about their contribution to soil C pools in the Brazilian Cerrado ( Justi et al., 2017Justi M, Schellekens J, Camargo PB, Vidal-Torrado P. Long-term degradation effect on the molecular composition of black carbon in Brazilian Cerrado soils. Org Geochem. 2017;113:196-209. https://doi.org/10.1016/j.orggeochem.2017.06.002
https://doi.org/10.1016/j.orggeochem.201...
). Thus, in ecosystems submitted to frequent fire, the dependence of soil C on belowground C inputs increases substantially ( Hoffmann and Franco, 2003Hoffmann WA, Franco AC. Comparative growth analysis of tropical forest and savanna woody plants using phylogenetically independent contrasts. J Ecol. 2003;91:475-84. https://doi.org/10.1046/j.1365-2745.2003.00777.x
https://doi.org/10.1046/j.1365-2745.2003...
), although some plants of the Cerrado allocate C belowground aiming to store water and nutrients in specialized organs ( Appezzato-da-Glória et al., 2008Appezzato-da-Glória B, Cury G, Soares MKM, Rocha R, Hayashi AH. Underground systems of Asteraceae species from the Brazilian Cerrado. J Torrey Bot Soc. 2008;135:103-13. https://doi.org/10.3159/07-RA-043.1
https://doi.org/10.3159/07-RA-043.1...
; Simon and Pennington, 2012Simon MF, Pennington T. Evidence for adaptation to fire regimes in the tropical savannas of the Brazilian Cerrado. Int J Plant Sci. 2012;173:711-23. https://doi.org/10.1086/665973
https://doi.org/10.1086/665973...
). In part of the Brazilian Cerrado and the Pampa, graminoids are favored by fire partially because they have a high capacity to resorb leaf nutrients and store them in their rhizomes ( Aerts, 1996Aerts R. Nutrient resorption from senescing leaves of perennials: Are there general patterns? J Ecol. 1996;84:597-608. https://doi.org/10.2307/2261481
https://doi.org/10.2307/2261481...
). Generally, the total belowground biomass in Cerrado grasslands is about 16.3 Mg ha–1 and can be as high as 52.9 Mg ha–1 in Cerrado forests ( Castro and Kauffman, 1998Castro EA, Kauffman JB. Ecosystem structure in the Brazilian Cerrado: a vegetation gradient of aboveground biomass, root mass and consumption by fire. J Trop Ecol. 1998;14:263-83. https://doi.org/10.1017/s0266467498000212
https://doi.org/10.1017/s026646749800021...
). Soil C pools under the Cerrado and the Amazon are quite similar, despite the huge difference in biomass production between them ( Figure 3 ). Hence, vegetation C pools are not a good indicator of the size of soil C pools in the tropics.

Overall, it can be inferred that i) vegetation C is much more sensitive to fire than soil C pools, ii) high NPP cannot be seen as an indicator of the size of soil C pools in tropical ecosystems, and iii) fire suppression may benefit soil C pools, but it comes at a cost of reduced plant biodiversity ( Abreu et al., 2017Abreu RCR, Hoffmann WA, Vasconcelos HL, Pilon NA, Rossatto DR, Durigan G. The biodiversity cost of carbon sequestration in tropical savanna. Sci Adv. 2017;3:e1701284. https://doi.org/10.1126/sciadv.1701284
https://doi.org/10.1126/sciadv.1701284...
). Similarly, liming and fertilization to sustain intensive agriculture with multiple crops grown in succession under no-tillage ( Pavinato et al., 2020Pavinato PS, Cherubin MR, Soltangheisi A, Rocha GC, Chadwick DR, Jones DL. Revealing soil legacy phosphorus to promote sustainable agriculture in Brazil. Sci Rep. 2020;10:15615. https://doi.org/10.1038/s41598-020-72302-1
https://doi.org/10.1038/s41598-020-72302...
) also should favor increasing soil C pools, particularly across the Cerrado. Based on the evidence gathered, in ecosystems where precipitation levels are low or suffer strong seasonality, high temperatures can override the control of MAP on EEM levels ( Figure 2 ). In line with these constraints, the C sink strength of Cerrado plants and remnants of the Pampa vegetation may be weakened by fire, whereas low NPP might play a bigger role across the Caatinga. In such biomes, vegetation C pools should not increase with temperature primarily because MAP levels are not high enough to control EEM.

Coupled decreases in temperature and precipitation levels

Across the SE-S transect of the Atlantic Forest domain, the reduction in precipitation is coincident with decreasing temperatures, allowing annual EEM to remain positive in this area ( Figure 2 ; Table 1 ). In these ecosystems, the relative C sink strength of vegetation and soils also can be framed by considering i) plant C allocation (e.g., above and belowground), ii) nutrients dynamics, and iii) the formation of mineral-organic associations.

In terms of plant C allocation, as both temperature and precipitation rates decrease, the reduced levels of soil water should force part of the plants growing under these constraints to shed their leaves to reduce transpiration ( Markesteijn et al., 2010Markesteijn L, Iraipi J, Bongers F, Poorter L. Seasonal variation in soil and plant water potentials in a Bolivian tropical moist and dry forest. J Trop Ecol. 2010;26:497-508. https://doi.org/10.1017/S0266467410000271
https://doi.org/10.1017/S026646741000027...
). This is a typical response of the semideciduous vegetation that occurs within the Atlantic Forest domain in Brazil ( Morellato et al., 2000Morellato LPC, Haddad CFB, Haddad CFB. Introduction: The Brazilian Atlantic Forest. Biotropica. 2000;32:786-92. https://doi.org/10.1111/j.1744-7429.2000.tb00618.x
https://doi.org/10.1111/j.1744-7429.2000...
). Quantitatively, between 25 and 50 % of the plants growing in semideciduous forests of the Atlantic Forest domain lose their leaves during the winter/dry season ( Arruda et al., 2018Arruda DM, Schaefer CEGR, Fonseca RS, Solar RRC, Fernandes Filho EI. Vegetation cover of Brazil in the last 21 ka: New insights into the Amazonian refugia and Pleistocenic arc hypotheses. Glob Ecol Biogeogr. 2018;27:47-56. https://doi.org/10.1111/geb.12646
https://doi.org/10.1111/geb.12646...
). Possibly, these plants also shed part of their roots as the soil moisture level decreases ( Kummerow et al., 1990Kummerow J, Castillanos J, Maas M, Larigauderie A. Production of fine roots and the seasonality of their growth in a Mexican deciduous dry forest. Vegetatio. 1990;90:73-80. https://doi.org/10.1007/BF00045590
https://doi.org/10.1007/BF00045590...
; Eissenstat and Yanai, 1997Eissenstat DM, Yanai RD. The ecology of root lifespan. Adv Ecol Res. 1997;27:1-60. https://doi.org/10.1016/s0065-2504(08)60005-7
https://doi.org/10.1016/s0065-2504(08)60...
; Campo et al., 1998Campo J, Jaramillo VJ, Maass JM. Pulses of soil phosphorus availability in a Mexican tropical dry forest: Effects of seasonality and level of wetting. Oecologia. 1998;115:167-72. https://doi.org/10.1007/s004420050504
https://doi.org/10.1007/s004420050504...
; Brunner et al., 2015Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C. How tree roots respond to drought. Front Plant Sci. 2015;6:547. https://doi.org/10.3389/fpls.2015.00547
https://doi.org/10.3389/fpls.2015.00547...
), but little is known about this aspect in most tropical ecosystems. This is certainly another subject that warrants further research. Given that 25 to 50 % of the plants in semideciduous forests lose their leaves during the cold-dry season, it is reasonable that 75 to 50 % of the vegetation can keep their leaves ( Arruda et al., 2018Arruda DM, Schaefer CEGR, Fonseca RS, Solar RRC, Fernandes Filho EI. Vegetation cover of Brazil in the last 21 ka: New insights into the Amazonian refugia and Pleistocenic arc hypotheses. Glob Ecol Biogeogr. 2018;27:47-56. https://doi.org/10.1111/geb.12646
https://doi.org/10.1111/geb.12646...
). Since EEM should decrease with decreasing precipitation ( Table 1 ), plants keeping their leaves must increase root growth to extract water from a larger volume of soil ( Markesteijn and Poorter, 2009Markesteijn L, Poorter L. Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought- and shade-tolerance. J Ecol. 2009;97:311-25. https://doi.org/10.1111/j.1365-2745.2008.01466.x
https://doi.org/10.1111/j.1365-2745.2008...
; Brunner et al., 2015Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C. How tree roots respond to drought. Front Plant Sci. 2015;6:547. https://doi.org/10.3389/fpls.2015.00547
https://doi.org/10.3389/fpls.2015.00547...
).

We posit that either plants shedding their leaves/roots or increasing root growth can contribute to explain the spatial distribution of soil C pools across the Atlantic Forest domain ( Figure 3 ). In the areas where plants shed their leaves, decreasing temperatures and precipitation combined may limit the mineralization rates of the plant litter added to the soil surface ( Sayer et al., 2006Sayer EJ, Tanner EVJ, Cheesman AW. Increased litterfall changes fine root distribution in a moist tropical forest. Plant Soil. 2006;281:5-13. https://doi.org/10.1007/s11104-005-6334-x
https://doi.org/10.1007/s11104-005-6334-...
). Owing to the negative correlation between MAT and EEM ( Figure 2 ; Table 1 ), these C inputs added to the soil surface should be less prone to fire ( Duff et al., 2018Duff TJ, Cawson JG, Harris S. Dryness thresholds for fire occurrence vary by forest type along an aridity gradient: evidence from Southern Australia. Landsc Ecol. 2018;33:1369-83. https://doi.org/10.1007/s10980-018-0655-7
https://doi.org/10.1007/s10980-018-0655-...
). Belowground, root-derived C inputs are added at greater soil depth and/or over a larger volume of soil ( Markesteijn et al., 2010Markesteijn L, Iraipi J, Bongers F, Poorter L. Seasonal variation in soil and plant water potentials in a Bolivian tropical moist and dry forest. J Trop Ecol. 2010;26:497-508. https://doi.org/10.1017/S0266467410000271
https://doi.org/10.1017/S026646741000027...
; Brunner et al., 2015Brunner I, Herzog C, Dawes MA, Arend M, Sperisen C. How tree roots respond to drought. Front Plant Sci. 2015;6:547. https://doi.org/10.3389/fpls.2015.00547
https://doi.org/10.3389/fpls.2015.00547...
). In contrast to the Amazon, where water fluxes through the soil profile can transport C towards the subsoil, plant C allocation into roots should be much more important for soil C pools across the domain of semideciduous vegetation of the Atlantic Forest. This inference also helps to explain why the correlation between soil C pools and clay content increases with depth ( Jobbágy and Jackson, 2000Jobbágy E, Jackson R. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl. 2000;10:423-36. https://doi.org/10.1890/1051-0761(2000)010%255B0423:TVDOSO%255D2.0.CO%253B2
https://doi.org/10.1890/1051-0761(2000)0...
). Although we have not considered clay content in our analysis, this factor should be considered in future studies. Apparently, in both ecosystems (Amazon and Atlantic Forest), plant feedbacks to climate exert a strong control on soil C pools, which responses are overwhelmingly opposite. As such, high MAP levels determine high EEM, which in turn favors vegetation C pools in the Amazon, whereas low winter temperature is critical for the occurrence of areas under positive EEM levels across the Atlantic Forest domain, where soil C pools are favored ( Figures 2 and 3 ). Consequently, whether precipitation or temperature exerts primary control on EEM has major effects on C pools’ size and its vertical partition in plant and soils. For instance, aboveground C pools can vary between 110–150 Mg ha–1 in humid ecosystems of the Atlantic Forest ( Vieira et al., 2011Vieira SA, Alves LF, Duarte-Neto PJ, Martins SC, Veiga LG, Scaranello MA, Picollo MC, Camargo PB, Carmo JB, Neto ES, Santos FAM, Joly CA, Martinelli LA. Stocks of carbon and nitrogen and partitioning between above-and belowground pools in the Brazilian coastal Atlantic Forest elevation range. Ecol Evol. 2011;1:421-34. https://doi.org/10.1002%2Fece3.41
https://doi.org/10.1002%2Fece3.41...
). Thus, the overall NPP and vegetation C pools in these areas are much lower than those observed across the Amazon domain ( Figure 3 ). The opposite is true for soil C, which pool corrected per unit area ( Gomes et al., 2019Gomes LC, Faria RM, Souza E, Veloso GV, Schaefer CEGR, Fernades Filho EI. Modelling and mapping soil organic carbon stocks in Brazil. Geoderma. 2019;340:337-50. https://doi.org/10.1016/j.geoderma.2019.01.007
https://doi.org/10.1016/j.geoderma.2019....
), is much lower across the Amazon than in the Atlantic Forest, at least in areas where EEM is positive. Another important aspect is that the Pampa shows EEM levels similar to those occurring across a SE-S transect of the Atlantic Forest ( Figure 2 ). However, soil C pools in the Pampa are very similar to those observed for the Cerrado. One possibility is that this pattern is caused by the summer dry season across the Pampa, where the highest EEM levels occur in the winter ( Figure 2 ).

We also infer that not only plant feedbacks to climate ultimately control the vertical partition of C in plants and soils, but also the persistence of soil C pools should depend on positive EEM. This is particularly relevant for mineral-organic associations, which are among the major drivers of the persistence of soil C pools ( Doetterl et al., 2015Doetterl S, Cornelis JT, Six J, Bodé S, Opfergelt S, Boeckx P, Van Oost K. Soil redistribution and weathering controlling the fate of geochemical and physical carbon stabilization mechanisms in soils of an eroding landscape. Biogeosciences. 2015;12:1357-71. https://doi.org/10.5194/bg-12-1357-2015
https://doi.org/10.5194/bg-12-1357-2015...
; Kleber et al., 2015Kleber M, Eusterhues K, Keiluweit M, Mikutta C, Mikutta R, Nico PS. Mineral–organic associations: Formation, properties, and relevance in soil environments. Adv Agron. 2015;130:1-140. https://doi.org/10.1016/bs.agron.2014.10.005
https://doi.org/10.1016/bs.agron.2014.10...
; Kramer and Chadwick, 2018Kramer MG, Chadwick OA. Climate-driven thresholds in reactive mineral retention of soil carbon at the global scale. Nat Clim Chang. 2018;8:1104-8. https://doi.org/10.1038/s41558-018-0341-4
https://doi.org/10.1038/s41558-018-0341-...
). Accordingly, mineral-organic associations primarily depend on i) moisture availability, ii) the presence of living plants; iii) active soil microbial biomass, iv) reactive minerals, and v) the acidification generated by the biotic factors involved ( Kleber et al., 2015Kleber M, Eusterhues K, Keiluweit M, Mikutta C, Mikutta R, Nico PS. Mineral–organic associations: Formation, properties, and relevance in soil environments. Adv Agron. 2015;130:1-140. https://doi.org/10.1016/bs.agron.2014.10.005
https://doi.org/10.1016/bs.agron.2014.10...
). In areas under Köppen C climates such as the Atlantic Forest, plants tend to produce leaf litter enriched in P, K, Ca, and Mg relative to plants growing under warm and humid climates (e.g., Köppen A) ( Vergütz et al., 2012Vergütz L, Manzoni S, Porporato A, Novais RF, Jackson RB. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr. 2012;82:205-20. https://doi.org/10.1890/11-0416.1
https://doi.org/10.1890/11-0416.1...
). Consequently, microbial C use efficiency should be favored by nutrient availability and cool Köppen C climates, with more microbial-derived products added into the soil C pool to form soil organic matter ( Singh et al., 1989Singh JS, Raghubanshi AS, Singh RS, Srivastava SC. Microbial biomass acts as a source of plant nutrients in dry tropical forest and savanna. Nature. 1989;338:499-500. https://doi.org/10.1038/338499a0
https://doi.org/10.1038/338499a0...
; Campo et al., 1998Campo J, Jaramillo VJ, Maass JM. Pulses of soil phosphorus availability in a Mexican tropical dry forest: Effects of seasonality and level of wetting. Oecologia. 1998;115:167-72. https://doi.org/10.1007/s004420050504
https://doi.org/10.1007/s004420050504...
; Manzoni et al., 2010Manzoni S, Trofymow JA, Jackson RB, Porporato A. Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr. 2010;80:89-106. https://doi.org/10.1890/09-0179.1
https://doi.org/10.1890/09-0179.1...
; Cotrufo et al., 2013Cotrufo MF, Wallenstein MD, Boot CM, Denef K, Paul E. The microbial efficiency-matrix stabilization (MEMS) framework integrates plant litter decomposition with soil organic matter stabilization: do labile plant inputs form stable soil organic matter? Glob Chang Biol. 2013;19:988-95. https://doi.org/10.1111/gcb.12113
https://doi.org/10.1111/gcb.12113...
). Otherwise, plants growing under Köppen C climates should resorb more C (+4.3 %) and N (+7.9 %) relative to plants growing under Köppen A climates ( Vergütz et al., 2012Vergütz L, Manzoni S, Porporato A, Novais RF, Jackson RB. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr. 2012;82:205-20. https://doi.org/10.1890/11-0416.1
https://doi.org/10.1890/11-0416.1...
). Although this pattern may be an indicator of the remobilization of C and N from senescing leaves to increase root growth during the cold/dry season, more research is needed on this topic.

Overall, leaf senescence and/or increased root growth may represent important pathways that regulate C inputs to soils in ecosystems dominated by semideciduous forests across the Atlantic Forest where the average annual EEM is positive. Thus, the transport of C by the percolating water should be much less relevant for soil C pools in these areas as compared to humid ecosystems occurring across the Amazon. Nonetheless, the persistence of soil C pools will ultimately depend on the mechanisms regulating C processing, such as microbial C use efficiency and its protection in mineral-organic associations.

Determinants of the ecosystem C pool: vegetation and soil as a function of climate constraints

Based on the evidence presented above and synthesized in table 2 , we propose a tentative conceptual model to describe the horizontal and vertical partition of C in plant-soil systems across the major Brazilian biomes ( Figure 4 ). Accordingly, as the precipitation level overrides the control of temperature on evapotranspiration and determines EEM levels, vegetation C pools are favored at the expense of a weak soil C sink. Such dynamics should be primarily relevant for the Amazon domain ( Figure 4 ), which covers approximately 50 % of the Brazilian territory. Otherwise, with increasing seasonality of precipitation, EEM is controlled by temperature, and consequently, vegetation C pools are weakened relative to soil C pools ( Figure 4 ). Thus, soil C can account for most of the ecosystem C pool because the vegetation C sink strength is weakened under high temperatures and low precipitation, as observed across the Caatinga, Cerrado, Pantanal, and Pampa (dry summer). Alternatively, decreasing temperatures limiting evapotranspiration allows positive EEM ( Figure 4 ), with some plants shedding their leaves and/or promoting deep rooting. In these areas, positive EEM levels also should favor mineral-organic associations, allowing the storage of C and nutrients in soil organic matter until increasing temperatures and precipitation favor their mineralization. This dynamic is probably more relevant for the mixed and semideciduous forests in the Atlantic Forest domain.

CONCLUSIONS

The enforcing effects of temperature and precipitation on Brazilian C pools are essentially hierarchical and can be quantitatively expressed by Ecosystem Effective Moisture (EEM). Accordingly, as precipitation rates increase, annual EEM levels are less affected by temperature and plants can trade more C for water. As a result, the vegetation C pool increases, but it depends on a weak soil C sink strength and fast mineralization rates of nutrients, especially P. With decreasing precipitation, EEM levels depend proportionally more on temperature. High temperatures reduce EEM, and vegetation C pools are limited by low net primary productivity (NPP), frequent fire and/or high nutrient losses. Decreasing temperatures allows EEM to remain positive even where precipitation undergoes seasonality, but plants either shed their leaves/roots or increase root production to explore a larger soil volume. Thus, the soil C sink is strengthened by the formation of mineral-organic associations, with more nutrients and microbial cell by-products stored in soil organic matter. Overall, the horizontal distribution of vegetation and soil C pools is best described by EEM, rather than temperature or precipitation alone. Likewise, the vertical partition of C in plant-soil systems reflects biotic responses to climate-nutrient constraints. Hence, the sensitivity of Brazilian C pools to temperature and its control on EEM should not be overlooked, especially as precipitation levels decrease. In other words, the projected increases in global temperatures and shifts in precipitation patterns may be relevant threats to Brazilian C pools.

ACKNOWLEDGEMENTS

The authors acknowledge the funding provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG), and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). IFS received funding from the Program CAPES–PNPD (process number 88887.356500/2019-00) and LCG received funding from the Program CAPES–PRINT (process number 88887.579255/2020-00). The authors also acknowledge the insightful comments from the anonymous reviewers who helped to correct and improve the manuscript.

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Edited by

Editors: José Miguel Reichert orcid.org/0000-0001-9943-2898 and Yuri Jacques Agra Bezerra da Silva orcid.org/0000-0001-6865-7146.

Publication Dates

  • Publication in this collection
    08 Dec 2021
  • Date of issue
    2021

History

  • Received
    12 July 2021
  • Accepted
    11 Oct 2021
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