Global Change Biology (2015) 21, 1752–1761, doi: 10.1111/gcb.12821

INVITED REVIEW

Mind the gap: non-biological processes contributing to soil CO2 efflux ANA REY Department of Biogeography and Global Change, National Museum of Natural Sciences (MNCN), Spanish Scientific Council (CSIC), C/Serrano 115, 28006 Madrid, Spain

Abstract Widespread recognition of the importance of soil CO2 efflux as a major source of CO2 to the atmosphere has led to active research. A large soil respiration database and recent reviews have compiled data, methods, and current challenges. This study highlights some deficiencies for a proper understanding of soil CO2 efflux focusing on processes of soil CO2 production and transport that have not received enough attention in the current soil respiration literature. It has mostly been assumed that soil CO2 efflux is the result of biological processes (i.e. soil respiration), but recent studies demonstrate that pedochemical and geological processes, such as geothermal and volcanic CO2 degassing, are potentially important in some areas. Besides the microbial decomposition of litter, solar radiation is responsible for photodegradation or photochemical degradation of litter. Diffusion is considered to be the main mechanism of CO2 transport in the soil, but changes in atmospheric pressure and thermal convection may also be important mechanisms driving soil CO2 efflux greater than diffusion under certain conditions. Lateral fluxes of carbon as dissolved organic and inorganic carbon occur and may cause an underestimation of soil CO2 efflux. Traditionally soil CO2 efflux has been measured with accumulation chambers assuming that the main transport mechanism is diffusion. New techniques are available such as improved automated chambers, CO2 concentration profiles and isotopic techniques that may help to elucidate the sources of carbon from soils. We need to develop specific and standardized methods for different CO2 sources to quantify this flux on a global scale. Biogeochemical models should include biological and nonbiological CO2 production processes before we can predict the response of soil CO2 efflux to climate change. Improving our understanding of the processes involved in soil CO2 efflux should be a research priority given the importance of this flux in the global carbon budget. Keywords: atmospheric pumping, carbonates, dissolved inorganic carbon, dissolved organic carbon, geological CO2, photodegradation, soil erosion, thermal convection Received 15 April 2014 and accepted 14 November 2014

Introduction Carbon stored in soils represents the largest carbon pool of terrestrial ecosystems with global estimates of organic pools of ca. 2400 Pg (Batjes, 1996; Jobbagy & Jackson, 2000). Soil carbon dynamics is therefore essential to predict the future global carbon balance. Soil CO2 efflux is the second largest flux of CO2 from terrestrial ecosystems to the atmosphere (Bond-Lamberty & Thomson, 2010a) with 10% of atmospheric CO2 cycling through soils annually (Reichstein & Beer, 2008). For this reason, research on this topic has been very active over the last few decades. In the current literature, soil CO2 efflux has been mostly assumed to be equivalent to soil respiration, that is, to biological activity within soils, but non-biological processes contribute to soil Correspondence: Ana Rey, tel. 0034 917452500 ext: 981162, fax 0034 915640800, e-mails: [email protected]; arey@mncn. csic.es

1752

CO2 efflux in many regions of the world (e.g. Rey et al., 2012a; Roland et al., 2013). Soil respiration is defined as the flux of CO2 resulting from the biological activity of roots, microfauna and microorganisms within the soil. Although the term soil CO2 efflux is often used, the flux of CO2 from soils is not the result of biological activity alone because other abiotic processes release CO2 as well. Many studies reporting soil CO2 efflux rates in several biomes, including temperate, boreal, tropical, Arctic and deserts have been published. This intense research has prompted excellent review summarizing methods (Kuzyakov, 2006; Subke et al., 2006; Bruggemann et al., 2011), processes (Smith et al., 2009; Kuzyakov & Gavrichkova, 2010; Kim et al., 2012), estimates for different biomes (Bond-Lamberty & Thomson, 2010a) and current challenges (Vargas et al., 2010a). Apart from evidencing great progress as well as limited understanding of the biological processes involved in soil respiration (Vargas et al., 2010a), non-biological © 2014 John Wiley & Sons Ltd

A B I O T I C P R O C E S S E S O F S O I L C O 2 P R O D U C T I O N 1753 processes contributing to soil CO2 efflux have not been considered in any of these synthesis papers. Specifically, some non-biological processes such as photodegradation, carbonate weathering reactions and the migration of geological CO2 originating in the subsoil to the surface of the soil that contribute to soil CO2 efflux in large regions of the planet have rarely been taken into account. Emission of CO2 from soils is the result of CO2 production in the soil and its transport to the atmosphere. Traditionally, research has focussed on the measurement of fluxes at the soil surface using a variety of chambers and micrometeorological methods. Thus, there is considerably less information available on CO2 dynamics below the soil surface although recently CO2 concentrations at different soil depths have been measured with the CO2 gradient method in several studies (e.g. Riveros-Iregui et al., 2008; Vargas et al., 2010b). Most current estimates are based on chamber methods and have assumed that the main mechanism of gas transport in soils is diffusion in air-filled pores, but other physical processes of mass transfer (i.e. advection) such as atmospheric pumping and temperaturedriven mass movement may also be important (Kuang et al., 2013; Ganot et al., 2014). Lateral losses of carbon in the form of dissolved organic and inorganic carbon in water may constitute an important carbon loss from ecosystems (Ciais et al., 2013) and affect soil CO2 efflux because part of the CO2 produced in soils gets lost in water. As a consequence, our understanding of the production and transport of CO2 in soils and how these processes are affected by changes in environmental and soil variables is rather poor. This study highlights certain key processes involved in soil CO2 efflux that have generally been neglected and that must be urgently addressed before we can reliably predict future trends in this important flux of carbon to the atmosphere. Specifically, we focus on non-biological processes that in some regions of the world may affect or contribute to soil CO2 efflux such as photodegradation, carbon exchange over carbonaceous substrates and geological gas (or geogas) emissions. Processes of CO2 transport within soils beyond soil CO2 diffusion, in particular atmospheric pumping, thermal convection, and lateral carbon losses, are also discussed. Beyond the importance of these processes on a global scale, failing to account for these processes may cause considerable errors in our estimates and assumptions about biologically produced soil CO2.

Processes of CO2 production Two major processes determine the CO2 efflux from soils: the production of CO2 within soils and its © 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761

transport and transfer across soils to the atmosphere (Fig. 1). Although it has generally been assumed that CO2 is produced within soils as a result of biological activity (Vargas et al., 2010a), various non-biological processes of CO2 production have recently been identified that may be important in many regions (Table 1).

Photodegradation One of the recent abiotic processes identified in drylands is the photochemical degradation of organic matter or photodegradation (Austin & Vivanco, 2006). Apart from the microbial breakdown of organic matter, photodegradation is an abiotic mechanism by which solar radiation breaks down chemical litter components releasing CO2 and changing the way nutrients and carbon are cycled among plants, soils and the atmosphere (King et al., 2012). A growing number of studies have shown that photodegradation plays a major role in surface litter decomposition in arid ecosystems (e.g. Austin & Vivanco, 2006; Gallo et al., 2006; Day et al., 2007; Brandt et al., 2009). Although there is considerable variation among and within ecosystems, a recent meta-analysis showed that overall litter exposed to solar radiation accelerates decomposition rates by 23% (King et al., 2012). However, the mechanisms for this mass loss remain unclear (Song et al., 2013). There are several mechanisms by which carbon could be lost via photodegradation: (1) facilitation of microbial decomposition through changes in litter chemistry to more labile components, (2) increased leaching losses of dissolved organic matter as a result of changes in litter solubility and (3) direct photochemical mineralization of litter releasing CO2 (Foereid et al., 2010). All of these mechanisms affect soil CO2 efflux rates. Furthermore, photodegradation has considerable implications for the carbon balance of an ecosystem as part of the carbon fixed in aboveground biomass is lost directly to the atmosphere or leached without cycling through soil organic matter pools (Rutledge et al., 2010; Smith et al., 2010). The incorporation of this process helps to explain discrepancies when applying soil carbon models of biotic control on litter decomposition in these regions. How this process will interact with other environmental factors (Caldwell et al., 2007; Smith et al., 2010), how it will indirectly affect microbial decomposition and diversity (e.g. Duguay & Klironomos, 2000) and litter quality (Austin & Ballar
e, 2010) and which factors control rates of photochemical CO2 production are all aspects that deserve further attention (Smith et al., 2010). Estimates of the amount of carbon loss through photodegradation in drylands could be substantial, with

1758 A . R E Y ecosystem carbon balance of a semiarid steppe. The geogas component depended on wind direction and intensity and amounted to almost 50% of the annual carbon balance. However, the emission of CO2 from deep sources, either from volcanic or geothermal areas, is often too heterogeneous for eddy covariance application in terms of the spatial and temporal variability of surface fluxes. A different approach coupling groundwater chemistry with hydrological and isotopic data was applied by Chiodini et al. (2004) to differentiate shallow vs. deep CO2 sources. In this study, the authors showed that in the tectonically active area of the Italian Apennines, approximately 40% of the inorganic carbon in groundwater derives from magmatic sources. Chiodini et al. (2008) developed a new method combining measurements of soil CO2 flux and determinations of the carbon isotopic composition of soil CO2 efflux to qualitatively and quantitatively characterize the CO2 source. Unravelling biological from geological carbon sources in soils is possible through the determination of the stable carbon isotope ratio 12C/13C of CO2. The isotopic signal of organic-derived material should have a signature very similar to the original plant, that is d13C:
24& to 38& (Pataki et al., 2003). The isotopic signature of geologically produced CO2 in geothermal–volcanic areas ranges from
8& to 0& (Jenden et al., 1993). Thus, the isotopic signal of soil CO2 efflux may give us a good insight into the origin of the CO2 released at the soil surface. However, as geological CO2 originated in sedimentary basins can be 13C-depleted (d13C <
15&) resembling the CO2 from soil respiration, radiocarbon (14C) analyses are sometimes necessary to recognize the geological component, which is 14C-free (fossil). The isotopic analyses should be combined with other deep-origin gaseous tracers, such as helium and methane [methane in normal soil conditions is typically below the atmospheric concentration, due to methanotrophic consumption, so high CH4 concentrations in dry soil may indicate the presence of geogas (Etiope & Klusman, 2010)]. Earth’s degassing is considered to be a relatively minor CO2 source globally in the order of 600–1000 Tg CO2 yr
1 (M€ orner & Etiope, 2002; Burton et al., 2013), but it is a major natural CH4 source (~54 Tg CH4 yr
1, i.e. about 10% of the total methane sources; Etiope, 2012; Ciais et al., 2013). Geo-CH4 and geo-CO2 may, however, affect surface ecosystem fluxes on wide areas and confound ecosystem carbon budgets attributed to biological activity leading to inaccurate estimates (Rey et al., 2014).

a strong soil–atmosphere concentration gradient that leads to net CO2 release into the atmosphere. So far, most studies assume that diffusion is the main mechanism driving this flux. However, in permeable, dry and fractured soils, advection processes driven by pressure and temperature gradients are also significant mechanisms of gas transport that have recently been identified as potentially important (Weisbrod et al., 2009; Kuang et al., 2013). Most current process-based models of soil carbon dynamics assume that CO2 migrates along the soil profile as a result of changes in CO2 concentration (Fick0 s law). However, models should also include other physical processes that may be important as well as lateral movement of CO2.

Transport processes

Thermal convection

As a result of the processes outlined above, CO2 accumulates in soil pore spaces causing the development of

Particularly in dryland continental areas that are characterized by large sensible heat fluxes, diurnal

Atmospheric pumping The fluctuations of atmospheric pressure induce gas movement between the atmosphere and soils from lowto high-pressure areas. This phenomenon is referred to as atmospheric pumping (Luo & Zhou, 2006). One of the main factors controlling advection transport is the amount of water in the soil, as it determines the degree of connectivity between the soil and the atmosphere and, thus, soil CO2 exchange. Other studies have also found that wind and pressure gradient differences drive soil CO2 effluxes (e.g. Tackle et al., 2004; Nachshon et al., 2012; Rey et al., 2012a). In permeable and fractured soils, this is the main mechanism of CO2 transport and thus of geological CO2 release. Soil cracks and fractures on the Earth’s surface are ubiquitous and are often found throughout arid, moist and cold climatic regions. Soil CO2 efflux has traditionally been measured with soil chambers placed on the ground. These chambers alter the soil–atmosphere interface, mostly removing wind, and therefore, they fail to capture this process. Pressure differences caused by wind are particularly effective for soil CO2 transport to the atmosphere (Rey et al., 2012a). Several studies have quantified this effect and have proven that chamber methods can induce errors in soil CO2 efflux (e.g. Bain et al., 2005), particularly in the presence of geogas (e.g. Rey et al., 2014). A combination of pressure measurements and CO2 concentration using the flux gradient method to measure CO2 concentrations at different soil depths should be more suitable to detect mass movement driven by atmospheric pumping as it does not alter the environmental conditions of soils or the soil–atmosphere interface.

© 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761

1. Production

Process

© 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761

1 mantle and magma degassing; 2 thermo-metamor phism of carbonate rocks (limestones); 3 thermogenesis during natural gas and oil production) in sedimentary basins

Carbonate weathering reactions: CaCO3 + CO2 + H2O ? Ca2 + +2HCO
3 (silicates) CaMg(CO3)2 + 2CO2 + 2H2O-Ca2 + Mg2+ + 4HCO
3 (dolomites) Mineral carbonation Ca/Mg (SiO3)2 + 2CO2 ? Ca/Mg (CaCO3)2 + 2SiO2 (peridotites) Endogenous CO2 migration from deep crustal rocks and Earth’s mantle

1.2 Pedochemical reactions

1.3 Geogas

Solar radiation breaks down organic matter (photochemical litter decomposition)

1.1 Photodegradation

Mechanism

Carbonaceous substrates (10% of world land surface) (Durr et al., 2005) 0.11–0.4 Gt yr
1 (Sarmiento & Sundquist, 1992; Liu & Zhou, 1999)

UV levels Soil moisture Relative humidity Litter quality Temperature Precipitation Leaf surface area Soil erosion Extreme climate events • Vegetation structure • Turbulent-driven mass transport • CO2 concentration fluctuations • pH • Soil moisture • Temperature • Water table fluctuations

• Turbulent-driven mass transport • Water table • Soil moisture • Seismic activity

• Stoichiometry of biochemical reactions • Pedochemical models • Isotopic signal of respired CO2 • CO2 concentration gradient • Eddy covariance in addition to accumulation chambers

• Geological inspection of the site • Isotopic signal of respired CO2 • CO2 concentration gradient method • Eddy covariance in addition to accumulation chambers • Statistical analysis of CO2 concentration and flux measurements

Volcanic and seismic areas High heat flow areas Fault areas 600–1000 Tg CO2 yr
1 (M€ orner & Etiope, 2002; Burton et al., 2013)

(Lee

26–78 Tg CO2–C yr et al., 2012) Mainly drylands

• • • • • • • • •


1

• Litter bags/litter boxes with UV filters • Direct gas exchange measurements with and without UV filters

Potential global significance

Main factors

Methods

Table 1 Main non-biological processes of soil CO2 production and CO2 transport

(1) Quantification of short-term and annual contribution to soil CO2 efflux in areas potentially affected by geofluid circulation and geogas emissions (2) Dependence on major environmental conditions and transport processes (3) Improved estimates at global scale (4) Incorporation into current process-based models

(1) Quantification of short-term and annual contribution to soil CO2 efflux over carbonate substrates (2) Characterization of dependence on major environmental conditions (3) Incorporation into current transport process-based models of soil CO2 efflux

(1) Indirect effect on microbial decomposition and diversity (2) Increased leaching of carbon (3) Direct CO2 release, contribution to litter decomposition and soil CO2 efflux (4) Contribution to soil CO2 efflux (5) Interaction with climate change drivers

Research needs

A B I O T I C P R O C E S S E S O F S O I L C O 2 P R O D U C T I O N 1755

Gas movement driven by atmospheric pressure variations, winds

Gas movement driven by temperature gradients

In water and by soil erosion

2.1 Atmospheric pumping

2.2 Thermal convection

2.3 Lateral DOC/ DIC/POC movement

Mechanism

Water balance equation Soil erosion rates Molecular characterization of dissolved organic matter

Theoretical air flow models Measurement of soil temperature gradients within soils CO2 concentration gradients

Theoretical air flow models

Methods

Potential global significance Important in fractured, porous media such as karstic systems, faults, shafts, caves, animal burrows

Particularly in cracked, fractured soils

Export to waters: 1.9 Pg C yr
1 (Cole et al., 2007)

Main factors • Changes in atmospheric pressure • Winds • Water table fluctuations • Soil moisture • Topography • Permeability of soils • Changes in air temperature • Water table • Soil moisture • Topography • Permeability of soils • Precipitation • Water drainage • Hydrological regimes • Throughfall • Ecosystem type • Extreme rainfall events

DIC, dissolved inorganic carbon; DOC, dissolved organic carbon; POC, particulate organic carbon.

2. Transport

Process

Table 1 (continued)

(1) Trace DOM origin as well as its transformations during transport (2) Greater understanding of factors controlling soil carbon mobilization to aquatic systems (3) Quantification of carbon loss through lateral losses for different ecosystems. (4) Quantification of fate of carbon: degassed waters, burial in sediments and export to the ocean.

(1) Impact on soil aeration and microbial activity. (2) Dependence on environmental variables to determine under which conditions prevail. (3) Contribution to soil CO2 efflux

(1) Characterization and quantification of this process. (2) Incorporation into current process-based models. (3) Impact on soil CO2 efflux

Research needs

1756 A . R E Y

© 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761

A B I O T I C P R O C E S S E S O F S O I L C O 2 P R O D U C T I O N 1757 (Schlesinger, 1982). Although its contribution to the annual soil carbon budget is small on medium- to long-time scales (Kuzyakov, 2006), it has been shown that on short-time scales (hourly–daily), the equilibrium of these reactions can be very dynamic explaining, under certain circumstances, diurnal patterns of soil CO2 exchange (Roland et al., 2013). Using a geochemical model to calculate weathering rates in a shrubland site in the SE of Spain, Roland et al. (2013) showed that weathering reactions can contribute considerably to the net ecosystem carbon balance during dry periods. As explained in this study, on carbonate substrates, changes in soil CO2 concentration within the soil–atmosphere caused by turbulence-driven mass transport affect the equilibrium of carbonate precipitation–dissolution reactions on short-time scales. Thus, weathering reactions should be taken into account when describing the temporal dynamics of soil CO2 efflux in carbonaceous substrates to enable the proper quantification of biologically produced CO2 in soils. Other recent studies carried out in dryland regions have reported anomalous CO2 flux patterns that could not be explained by biological activity (e.g. Schlesinger et al., 2009; Serrano-Ortiz et al., 2010; Chen et al., 2014) including CO2 effluxes that are much larger than expected from vegetation activity or even CO2 uptake at night (Kowalski et al., 2008). Carbonate substrates cover more than 10% of the world’s land surface (Durr et al., 2005), so the contribution of carbonate weathering to soil CO2 efflux, although small, needs to be considered to properly quantify biologically produced soil CO2 efflux. Current estimates of the net contribution of carbonate rock weathering ranged from 0.11 (Liu & Zhou, 1999) to 0.4 Gt of C yr
1 (Sarmiento & Sundquist, 1992). Given that there are well-known pedochemical reactions (Berner et al., 1983; Kaufmann & Dreybrodt, 2007), the use of biochemical models and environmental variables should allow these processes to be easy calculated so that they can be explicitly included in current mechanistic soil CO2 efflux models. Other non-carbonate substrates such as peridotites (ultramafic rocks) interact with soil CO2 through mineral carbonation, which has been proposed as a potential mechanism of carbon sequestration (Matter & Kelemen, 2009). Mineral carbonation involves the reaction of CO2 with non-carbonate minerals to form stable mineral carbonates. This process occurs under natural conditions and may affect the flux of CO2 from soils in these areas. CO2 uptake by near-surface carbonation has been estimated to be ~103 tons of CO2 km
3 yr
by peridotite carbonation in Oman (Kelemen & Matter, 2008). © 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761

Geological CO2 fluxes Another potentially important non-biological CO2 source in soils is geological CO2, that is, an endogenous CO2 migration from deep crustal rocks or even from the Earth’s mantle. Geological CO2 may have various origins, ranging from magma degassing and thermometamorphism of carbonates (limestones) in geothermal and volcanic areas, to the thermal maturity of organic matter (thermogenesis during natural gas and oil production, also known as kerogen decarboxylation) or hydrocarbon oxidation and biodegradation in petroleum-bearing sedimentary basins (e.g. Jenden et al., 1993; Etiope et al., 2009). Gas migration typically occurs along tectonic faults. On the Earth’s surface, this geogas can produce visible manifestations (e.g. mofettes, bubbling springs, CO2-rich mud volcanoes), but in most cases, throughout vast regions of the planet, the exhalation is invisible and mixes with soil biologically produced gas (M€ orner & Etiope, 2002; Burton et al., 2013). This geogas is not exclusive to active volcanic–geothermal regions; high geo-CO2 fluxes have also been measured in tectonically active and seismic areas, independently from the geothermal heat flow (M€ orner & Etiope, 2002; Chiodini et al., 2004). A recent study by Rey et al. (2012a) hypothesized the existence of a non-biological CO2 source contributing to the net ecosystem carbon balance of a semiarid steppe in the SE of Spain. As the study area was located over a tectonic fault in an ancient volcanic area (the main volcanic district of Spain), it was hypothesized that geological CO2 sources contributed to the net ecosystem carbon balance. A follow-up study (Rey et al., 2012b) demonstrated this hypothesis using isotopic carbon analyses of CO2 in water, air and soil CO2 efflux at the site and nearby. These studies highlighted the potential importance of considering geological CO2 sources when ecosystems are located in geothermal and faulted areas. The geogas CO2, that in petroliferous sedimentary basins is associated with methane (CH4), actually exhales to the surface mixing with soil respiration over large areas (e.g. Etiope, 1999, 2012; Lewicki et al., 2003; Chiodini et al., 2008; Etiope et al., 2011). Even though the existence of the diffused emission of geogas is well known among geologists and geochemists, ecologists have mostly ignored it. Only recently has geogas emission been included in European and global carbon budgets (e.g. Schulze et al., 2011; Luyssaert et al., 2012). Eddy covariance has recently been proposed as a method to monitor volcanic CO2 emissions (Werner & Brantley, 2003). Rey et al. (2014) used eddy covariance data together with physical parameters of the boundary layer to derive the geological contribution to the net

1758 A . R E Y ecosystem carbon balance of a semiarid steppe. The geogas component depended on wind direction and intensity and amounted to almost 50% of the annual carbon balance. However, the emission of CO2 from deep sources, either from volcanic or geothermal areas, is often too heterogeneous for eddy covariance application in terms of the spatial and temporal variability of surface fluxes. A different approach coupling groundwater chemistry with hydrological and isotopic data was applied by Chiodini et al. (2004) to differentiate shallow vs. deep CO2 sources. In this study, the authors showed that in the tectonically active area of the Italian Apennines, approximately 40% of the inorganic carbon in groundwater derives from magmatic sources. Chiodini et al. (2008) developed a new method combining measurements of soil CO2 flux and determinations of the carbon isotopic composition of soil CO2 efflux to qualitatively and quantitatively characterize the CO2 source. Unravelling biological from geological carbon sources in soils is possible through the determination of the stable carbon isotope ratio 12C/13C of CO2. The isotopic signal of organic-derived material should have a signature very similar to the original plant, that is d13C:
24& to 38& (Pataki et al., 2003). The isotopic signature of geologically produced CO2 in geothermal–volcanic areas ranges from
8& to 0& (Jenden et al., 1993). Thus, the isotopic signal of soil CO2 efflux may give us a good insight into the origin of the CO2 released at the soil surface. However, as geological CO2 originated in sedimentary basins can be 13C-depleted (d13C <
15&) resembling the CO2 from soil respiration, radiocarbon (14C) analyses are sometimes necessary to recognize the geological component, which is 14C-free (fossil). The isotopic analyses should be combined with other deep-origin gaseous tracers, such as helium and methane [methane in normal soil conditions is typically below the atmospheric concentration, due to methanotrophic consumption, so high CH4 concentrations in dry soil may indicate the presence of geogas (Etiope & Klusman, 2010)]. Earth’s degassing is considered to be a relatively minor CO2 source globally in the order of 600–1000 Tg CO2 yr
1 (M€ orner & Etiope, 2002; Burton et al., 2013), but it is a major natural CH4 source (~54 Tg CH4 yr
1, i.e. about 10% of the total methane sources; Etiope, 2012; Ciais et al., 2013). Geo-CH4 and geo-CO2 may, however, affect surface ecosystem fluxes on wide areas and confound ecosystem carbon budgets attributed to biological activity leading to inaccurate estimates (Rey et al., 2014).

a strong soil–atmosphere concentration gradient that leads to net CO2 release into the atmosphere. So far, most studies assume that diffusion is the main mechanism driving this flux. However, in permeable, dry and fractured soils, advection processes driven by pressure and temperature gradients are also significant mechanisms of gas transport that have recently been identified as potentially important (Weisbrod et al., 2009; Kuang et al., 2013). Most current process-based models of soil carbon dynamics assume that CO2 migrates along the soil profile as a result of changes in CO2 concentration (Fick0 s law). However, models should also include other physical processes that may be important as well as lateral movement of CO2.

Transport processes

Thermal convection

As a result of the processes outlined above, CO2 accumulates in soil pore spaces causing the development of

Particularly in dryland continental areas that are characterized by large sensible heat fluxes, diurnal

Atmospheric pumping The fluctuations of atmospheric pressure induce gas movement between the atmosphere and soils from lowto high-pressure areas. This phenomenon is referred to as atmospheric pumping (Luo & Zhou, 2006). One of the main factors controlling advection transport is the amount of water in the soil, as it determines the degree of connectivity between the soil and the atmosphere and, thus, soil CO2 exchange. Other studies have also found that wind and pressure gradient differences drive soil CO2 effluxes (e.g. Tackle et al., 2004; Nachshon et al., 2012; Rey et al., 2012a). In permeable and fractured soils, this is the main mechanism of CO2 transport and thus of geological CO2 release. Soil cracks and fractures on the Earth’s surface are ubiquitous and are often found throughout arid, moist and cold climatic regions. Soil CO2 efflux has traditionally been measured with soil chambers placed on the ground. These chambers alter the soil–atmosphere interface, mostly removing wind, and therefore, they fail to capture this process. Pressure differences caused by wind are particularly effective for soil CO2 transport to the atmosphere (Rey et al., 2012a). Several studies have quantified this effect and have proven that chamber methods can induce errors in soil CO2 efflux (e.g. Bain et al., 2005), particularly in the presence of geogas (e.g. Rey et al., 2014). A combination of pressure measurements and CO2 concentration using the flux gradient method to measure CO2 concentrations at different soil depths should be more suitable to detect mass movement driven by atmospheric pumping as it does not alter the environmental conditions of soils or the soil–atmosphere interface.

© 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761

A B I O T I C P R O C E S S E S O F S O I L C O 2 P R O D U C T I O N 1759 temperature gradients are often considerable, and thermal convection, that is the air movement driven by temperature gradients, is another important mechanism of gas transfer in soils. Ganot et al. (2014) showed that on highly permeable soils, the thermal convective transport of CO2 could override CO2 diffusion processes and significantly enhance CO2 transport. Tackle et al. (2004) reported CO2 fluxes over a bare field and found mean soil CO2 flux rates that were about 5–10 times greater than Fick0 s diffusion predictions; and three- to sevenfold rates greater than those attributable to pressure pumping effects suggesting thermal expansion of soil air as an additional mechanism of CO2 transport in soils. This thermal convection mechanism of soil CO2 vertical movement has rarely been considered, but it is likely to play a major role with rates two orders of magnitude greater than diffusive processes in certain cases (Ganot et al., 2014). In dryland soils, which have been much less studied, all or some of these processes may be involved in soil CO2 efflux, but so far, no specific studies have quantified their relative importance or their temporal and spatial variation.

Lateral CO2 losses In most studies, it is assumed that CO2 travels vertically from soils to the atmosphere, but lateral fluxes of organic and inorganic carbon between soils and aquatic systems also occur. Traditionally, studies generally focus on the temporal variability of soil CO2 efflux (diel, seasonal and annual variability, e.g. Rey et al., 2002; Vargas et al., 2010c) and spatial variability (e.g. Rodeghiero & Cescatti, 2008; Luo et al., 2012), but few studies have quantified lateral losses. Failing to account for dissolved organic carbon (DOC) fluxes underestimates the amount of carbon attributed to soil CO2 dynamics because part of the carbon produced migrates to aquatic systems (Wang et al., 2014). Siemens (2003) suggested DOC fluxes as a possible explanation for the observed gap between atmosphere-based and land-based estimates of the continental carbon balance of Europe (Janssens et al., 2003). Considerable uncertainties surrounded the quantity of carbon mobilized from soils, released into the atmosphere during river transport and delivered to the ocean (Cole et al., 2007; Raymond et al., 2013). Although presumably of small magnitude, it has been estimated that these fluxes could be of great importance in the global carbon cycle (Battin et al., 2009). On a local scale, they may cause an underestimation of the soil CO2 produced. Other forms of carbon loss in water include particulate organic carbon (POC) and dissolved inorganic carbon (DIC). Ciais et al. (2008) estimated that POC © 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761

represents 8% of total organic carbon (TOC) across Northern Europe. Luyssaert et al. (2010) reported an average DOC leaching of 10 g C m
2 yr
1 for all terrestrial ecosystems. These lateral losses vary temporally as well as among ecosystems and landscapes according to hydrological conditions as water drainage and precipitation are the major factors controlling these fluxes. Besides lateral carbon losses in water, soil erosion is yet another process by which fresh and more labile carbon gets redistributed in landscapes also as DOC (Zhang et al., 2006; Berhe et al., 2012). The quantitative importance and the fate of this organic carbon have rarely been studied. Soil erosion drastically influences not only the lateral SOC distribution within a landscape but also soil CO2 fluxes to the atmosphere (Lal, 2003). Van Oost et al. (2007) summarized at least three key mechanisms affecting soil CO2 efflux: (1) loss of SOC at the eroding sites, (2) deep burial of SOC-rich topsoils at depositional sites and (3) enhanced decomposition of SOC through the chemical or physical breakdown of soil during detachment and transport (Lal, 2003). The amount of carbon lost in water drainage could be calculated with a water balance equation using evapotranspiration (ET) (as measured by eddy covariance or other methods), precipitation and soil water content (SWC).

Conclusions Beyond the uncertainty that still exists regarding the relative contribution of the different components of biologically produced CO2 in soils (autotrophic and heterotrophic respiration), we have identified other non-biological sources involved in soil CO2 efflux that have not yet received sufficient enough attention in the current literature: in particular photodegradation, carbon exchange over carbonaceous substrates and geological gas emissions. Although these processes are well known, they have rarely been taken into account in soil CO2 efflux studies. We should think about soils as the interface between the geosphere, pedosphere, hydrosphere, biosphere and atmosphere and characterize CO2 exchange among them for an accurate estimation of this important flux into the atmosphere. Apart from their importance on a global scale, these processes may contribute to soil CO2 efflux in many areas of the planet and confound our estimates of soil biological activity. Many of the processes described may be of particular relevance in drylands, which occupy more than 43% of the Earth and are much less studied than other biomes (Schimel, 2010). New methods including continuous measurements using automated chambers to capture the high-resolution temporal dynamics of soil CO2 efflux (e.g.

1760 A . R E Y Koskinen et al., 2014), CO2 concentration profiles that allow the calculation of soil CO2 efflux without altering the soil–atmosphere interface (e.g. Riveros-Iregui et al., 2008) and isotopic techniques to quantify different CO2 sources (e.g. Chiodini et al., 2008) can help to discern between different processes. As has been done with gap filling and data processing for eddy covariance data within the FLUXNET community, soil CO2 efflux methods should be standardized to account for all the processes involved in CO2 production and transport. This is the way forward to integrate measurements and to obtain reliable global estimates. Investigating the sources of CO2 emitted from soils and the factors controlling them is essential for understanding soil carbon exchange and ultimately to quantify the global carbon cycle. Before we can predict future impacts of climate change on soil CO2 efflux and soil carbon processes, we should improve current process-based models, separate production and transport processes and describe the different components of soil CO2 efflux and how they respond to environmental variables. The complexity of the processes involved in soil CO2 efflux requires enhanced interdisciplinary communication, in particular between microbial ecologists, biogeochemists, geologists, hydrologists, soil physicists and plant ecophysiologists.

Acknowledgements I thank Dr Etiope from the INGV in Rome for helpful discussion and useful comments on the manuscript and Prof. Valladares from MNCN in Madrid and Catherine MacBeth for proof editing the manuscript. I thank three anonymous reviewers and Global Change Biology for inviting me to write this manuscript and helping me with the process. The Ministry of Economy and Competitiveness of Spain, Project CGL2011-24748 supported this work.

References Austin AT, Ballar
e CL (2010) Dual role of lignin in litter decomposition in terrestrial ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 107, 4618–4622. Austin AT, Vivanco L (2006) Plant litter decomposition in a semi-arid ecosystem controlled by photodegradation. Nature, 442, 555–558. Bain WG, Hutyra L, Patterson DC et al. (2005) Wind-induced error in the measurement of soil respiration using closed dynamic chambers. Agricultural & Forest Meteorology, 131, 225–232. Batjes NH (1996) Total carbon and nitrogen in the soils of the world. European Journal of Soil Science., 47, 151–163. Battin TJ, Luyssaert S, Kaplan LA et al. (2009) The boundless carbon cycle. Nature Geoscience, 2, 598–600. Berhe AA, Harden JW, Torn MS et al. (2012) Persistence of soil organic matter in eroding versus depositional landform positions. Journal of Geophysical Research Biogeosciences, 117, G02019. Berner RA, Lasaga AC, Garrels RM (1983) The carbonate-silicate geochemical cycle and its effect on atmospheric carbon-dioxide over the past hundred million years. American Journal of Science, 283, 641–683. Bond-Lamberty B, Thomson A (2010a) Temperature-associated increases in the global soil respiration record. Nature, 464, 579–582.

Bond-Lamberty B, Thomson A (2010b) A global database of soil respiration data. Biogeosciences, 7, 1915–1926. Brandt LA, Bohnet C, King JY (2009) Photochemically induced carbon dioxide production as a mechanism for carbon loss from plant litter in arid ecosystems. Journal of Geophysical Research Biogeosciences, 114, G02004. Bruggemann N, Gessler A, Kayler Z et al. (2011) Carbon allocation and carbon isotope fluxes in the plant-soil-atmosphere continuum: a review. Biogeosciences, 8, 3457– 3489. Burton MR, Sawyer GM, Granieri D (2013) Deep carbon emissions from volcanoes. Reviews in Mineralogy and Geochemistry, 75, 323–354. Caldwell MM, Bornman JF, Ballar
e CL et al. (2007) Terrestrial ecosystems, increased solar ultraviolet radiation, and interactions with other climate change factors. Photochemical & Photobiological Sciences: Official Journal of the European Photochemistry Association and the European Society for Photobiology, 46, 40–52. Canadell JG, Le Quer
e C, Raupach MR et al. (2007) Contributions to accelerating atmospheric CO2 growth from economic activity, carbon intensity, and efficiency of natural sinks. Proceedings of the National Academy of Sciences of the United States of America, 104, 18866–18870. Chen X, Wang WF, Luo GP et al. (2014) Can soil respiration estimate neglect the contribution of abiotic exchange? Journal of Arid Environments, 6, 129–135. Chiodini G, Cardellini C, Amato A et al. (2004) Carbon dioxide Earth degassing and seismogenesis in central and southern Italy. Geophysical Research Letters, 31, L07615. Chiodini G, Caliro S, Cardellini C et al. (2008) Carbon isotopic composition of soil CO2 efflux, a powerful method to discriminate different sources feeding soil CO2 degassing in volcanic-hydrothermal areas. Earth Planetary Science Letters, 274, 372– 379. Ciais P, Borges AV, Abril G et al. (2008) The impact of lateral carbon fluxes on the European carbon balance. Biogeosciences, 5, 1259–1271. Ciais P, Sabine C, Bala G et al. (2013) Carbon and other biogeochemical cycles. In: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of IPCC (eds Stocker TF et al.). Cambridge University Press, Cambridge, UK and New York, NY, USA. Cole JJ, Prairie YT, Caraco NF et al. (2007) Plumbing the global carbon cycle: integrating inland waters into the terrestrial carbon budget. Ecosystems, 10, 171–184. Day TA, Zhang ET, Rahland CT (2007) Exposure to solar UV-B radiation accelerates mass and lignin loss of Larrea tridentata litter in the Sonoran Desert. Plant Ecology, 193, 185–194. Duguay KJ, Klironomos JN (2000) Direct and indirect effects of enhanced UV-B radiation on the decomposing and competitive abilities of saprobic fungi. Applied Soil Ecology, 14, 157–164. Durr HH, Meybeck M, Derr SH (2005) Lithologic composition of the Earth0 s continental surface derived from a new digital map emphasizing riverine material transfer. Global Biogeochemical Cycles, 19, GB4s00. Etiope G (1999) Subsoil CO2, and CH4 and their advective transfer from faulted grassland to the atmosphere. Journal of Geophysical Research, 104 (D14), 16889–16894. Etiope G (2012) Methane uncovered. Nature Geosciences, 5, 373–374. Etiope G, Klusman RW (2010) Microseepage in drylands: flux and implications in the global atmospheric source/sink budget of methane. Global and Planetary Change, 72, 265–274. Etiope G, Feyzullayev A, Milkov AV et al. (2009) Evidence of subsurface anaerobic biodegradation of hydrocarbons and potential secondary methanogenesis in terrestrial mud volcanoes. Marine and Petroleum Geology, 26, 1692–1703. Etiope G, Nakada R, Tanaka K et al. (2011) Gas seepage from Tokamachi mud volcanoes, onshore Niigata Basin (Japan): origin, post-genetic alterations and CH4-CO2 fluxes. Applied Geochemistry, 26, 348–359. Foereid B, Bellarby J, Meier-Augenstein W et al. (2010) Does light exposure make plant litter more degradable? Plant and Soil, 333, 275–285. Gallo ME, Sinsabaugh RL, Cabaniss SE (2006) The role of ultraviolet radiation in litter decomposition in arid ecosystems. Applied Soil Ecology, 34, 82–91. Ganot Y, Dragilab MI, Weisbrod N (2014) Impact of thermal convection on CO2 flux across the earth–atmosphere boundary in high-permeability soils. Agricultural and Forest Meteorology, 184, 12–24. Janssens IA, Freibauer A, Ciais P et al. (2003) Europe’s terrestrial biosphere absorbs 7 to 12% of European anthropogenic CO2 emissions. Science, 300, 1538–1542. Jenden PD, Hilton DR, Kaplan IR, Craig H (1993) Abiogenic hydrocarbons and mantle helium in oil and gas fields. In: The Future of Energy Gases (US Geological Survey Professional Paper 1570) (ed. Howell DG), pp. 31–56. United States Government Printing Office, Washington, DC. Jobbagy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecological Applications, 10, 423–436.

© 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761

A B I O T I C P R O C E S S E S O F S O I L C O 2 P R O D U C T I O N 1761 Kaufmann G, Dreybrodt W (2007) Calcite dissolution kinetics in the system CaCO3-H2O-CO2 at high undersaturation. Geochimica et Cosmochimica Acta, 71,

Rey A, Belelli-Marchesini L, Etiope G et al. (2014) Partitioning the net ecosystem carbon balance of a semiarid steppe into biological and geological carbon compo-

1398–1410. Kelemen PB, Matter J (2008) In situ carbonation of peridotite for CO2 storage. Proceedings of the National Academy of Sciences of the United States of America, 105, 17295– 17300. Kim R, Vargas R, Bond-Lamberty B et al. (2012) Effects of soil rewetting and thawing on soil gas fluxes: a review of current literature and suggestions for future research. Biogeosciences, 9, 2459–2483.

nents. Biogeochemistry, 118, 83–101. Riveros-Iregui DA, McGlynn BL, Epstein HE et al. (2008) Interpretation and evaluation of combined measurement techniques for soil CO2 efflux: discrete surface chambers and continuous soil CO2 concentration probes. Journal of Geophysical Research, 113, G04027. Rodeghiero M, Cescatti A (2008) Spatial variability and optimal sampling strategy of soil respiration. Forest Ecology and Management, 255, 106–112.

King AW, Hayes DJ, Huntzinger DN et al. (2012) North American carbon dioxide sources and sinks: magnitude, attribution, and uncertainty. Frontiers in Ecology and the Environment, 10, 512–519. Koskinen M, Minkkinen K, Ojanen P et al. (2014) Measurements of CO2 exchange with an automated chamber system throughout the year: challenges in measuring night-time respiration on porous peat soil. Biogeosciences, 11, 347–363.

Roland M, Serrano-Ortiz P, Kowalski AS et al. (2013) Atmospheric turbulence triggers pronounced diel pattern in karst carbonate geochemistry. Biogeosciences, 10, 5009– 5017. Rutledge S, Campbell DJ, Baldocchi D et al. (2010) Photodegradation leads to increased carbon dioxide losses from terrestrial organic matter. Global Change Biology, 16, 3065–3074.

Kowalski AS, Serrano-Ortiz P, Janssens IA et al. (2008) Can flux tower research neglect geochemical CO2 exchange? Agricultural and Forest Meteorology, 148, 1045– 1054. Kuang X, Jiao JJ, Li H (2013) Review on airflow in unsaturated zones induced by natural forcings. Water Resources Research, 49, 6137–6165. Kuzyakov Y (2006) Sources of CO2 efflux from soil and review of partitioning methods. Soil, Biology and Biochemistry, 38, 425–448.

Sarmiento JL, Sundquist ET (1992) Revised budget for the oceanic uptake of anthropogenic carbon dioxide. Nature, 356, 589–593. Schimel DS (2010) Climate. Drylands in the Earth system. Science, 327, 418–419. Schlesinger WH (1982) Carbon storage in the caliche of the arid world: a case study from Arizona. Soil Science, 133, 247–255. Schlesinger WH, Belnap J, Marion G (2009) On carbon sequestration in desert ecosystems. Global Change Biology, 15, 1488–1490.

Kuzyakov Y, Gavrichkova O (2010) Time lag between photosynthesis and carbon dioxide efflux from soil: a review of mechanisms and controls. Global Change Biology, 16, 3386–3406. Lal R (2003) Soil erosion and the global carbon budget. Environment International, 29, 437–450. Lee H, Rahn T, Throop H (2012) An accounting of C-based trace gas release during

Schulze ED, Luyssaert S, Ciais P et al. (2011) Importance of methane and nitrous oxide for Europe’s terrestrial greenhouse-gas balance. Nature Geosciences, 2, 842– 850. Serrano-Ortiz P, Roland M, Sanchez-Moral S et al. (2010) Hidden, abiotic CO2 flows and gaseous reservoirs in the terrestrial carbon cycle: review and perspectives. Agricultural and Forest Meteorology, 150, 321–329.

abiotic plant litter degradation. Global Change Biology, 18, 1185–1195. Lewicki JL, Evans WC, Hilley GE et al. (2003) Shallow soil CO2 flow along the San Andreas and Calaveras Faults, California. Journal of Geophysical Research, 108, 2187. Liu Z, Zhou J (1999) Contribution of carbonate rock weathering to the atmospheric CO2 sink. Environmental Geology, 39, 1053–1058. Luo Y, Zhou X (2006) Soil Respiration and the Environment. Academic Press, Elsevier.

Siemens J (2003) The European carbon budget: a gap. Science, 302, 1681. Smith WK, Gao W, Steltzer H (2009) Current and future impacts of ultraviolet radiation on the terrestrial carbon balance. Frontiers in Earth Science China, 3, 34–41. Smith WK, Gao W, Steltzer H et al. (2010) Moisture availability influences the effect of ultraviolet-B radiation on leaf litter decomposition. Global Change Biology, 16, 484–495. Song X, Peng C, Jiang H et al. (2013) Direct and indirect effects of UV-B exposure on

Luo J, Chen Y, Wu W et al. (2012) Temporal-spatial variation and controls of soil respiration in different primary succession stages on glacier forehead in Gongga Mountain, China. Plos One, 7, e42354. Luyssaert S, Ciais P, Piao SL et al. (2010) The European carbon balance. Part 3: forests. Global Change Biology, 16, 1429–1450. Luyssaert S, Abril G, Andres R et al. (2012) The European land and inland water CO2,

litter decomposition: a meta-analysis. PLoS One, 8, e68858. Subke J-A, Inglima I, Cotrufo MF (2006) Trends and methodological impacts in soil CO2 efflux partitioning: a metaanalytical review. Global Change Biology, 12, 921– 943. Tackle ES, Massman WJ, Brandle JR et al. (2004) Influence of high-frequency ambient pressure pumping on carbon dioxide efflux from soil. Agricultural and Forest Meteo-

CO, CH4 and N2O balance between 2001 and 2005. Biogeosciences, 9, 3357–3380. Matter JM, Kelemen PB (2009) Permanent storage of carbon dioxide in geological reservoirs by mineral carbonation. Nature Geoscience, 2, 837–841. M€ orner NA, Etiope G (2002) Carbon degassing from the lithosphere. Global and Planetary Change, 33, 185–203. Nachshon U, Dragila M, Weisbrod N (2012) From atmospheric winds to fracture ventilation: cause and effect. Journal of Geophysical Research, 117, G02016.

rology, 124, 193–206. Van Oost K, Quine TA, Govers G et al. (2007) The impact of agricultural soil erosion on the global carbon cycle. Science, 318, 626–629. Vargas R, Carbone MS, Reichstein M et al. (2010a) Frontiers and challenges in soil respiration research: from measurements to model-data integration. Biogeochemistry, 102, 1–13. Vargas R, Detto M, Baldocchi DD et al. (2010b) Multiscale analysis of temporal vari-

Pataki DE, Ehleringer JR, Flanagan L-B et al. (2003) The application and interpretation of Keeling plots in terrestrial carbon cycle research. Global Biogeochemical Cycles, 17. doi: 10.1029/2001GB001850. Raymond PA, Hartmann J, Lauerwald R et al. (2013) Global carbon dioxide emissions from inland waters. Nature, 503, 355–359. Reichstein M, Beer C (2008) Soil respiration across scales: the importance of a model-

ability of soil CO2 production as influenced by weather and vegetation. Global Change Biology, 16, 1589–1605. Vargas R, Baldocchi DD, Allen MF et al. (2010c) Looking deeper into the soil: biophysical controls and seasonal lags of soil CO2 production and efflux. Ecological Applications, 20, 1569–1582. Wang X, Cammeraat ELH, Romeijn P et al. (2014) Soil organic carbon redistribution

data integration framework for data interpretation. Journal of Plant Nutrition and Soil Science, 171, 344–354. Rey A, Pegoraro E, Tedeschi V et al. (2002) Seasonal variability in soil respiration and its components in a coppice oak forest in central Italy. Global Change Biology, 8, 1–18. Rey A, Belelli-Marchesini L, Were A et al. (2012a) Wind as the main driver of net ecosystem carbon balance of a semiarid steppe ecosystem in the SE of Spain. Global Change Biology, 18, 539–554.

by water erosion – The role of CO2 emissions for the carbon budget. PLoS One, 9, e96299. Weisbrod N, Dragila MI, Nachshon U et al. (2009) Falling through the cracks: the role of fractures in Earth-atmosphere gas exchange. Geophysical Research Letters, 36, L02401. Werner C, Brantley S (2003) CO2 emissions from the Yellowstone volcanic system. Geochemistry, Geophysics and Geosystems, 7, 1061. doi: 10.1029/2002GC000473.

Rey A, Etiope G, Belelli-Marchesini L et al. (2012b) Geological carbon sources may confound ecosystem carbon balance estimates: evidence from a semiarid steppe in the SE of Spain. Journal of Geophysical Research, 117, G03034.

Zhang JH, Quine TA, Ni SJ, Ge FL (2006) Stocks and dynamics of SOC in relation to soil redistribution by water and tillage erosion. Global Change Biology, 12, 1834– 1841.

© 2014 John Wiley & Sons Ltd, Global Change Biology, 21, 1752–1761