REVIEW Oxygen diffusion in soils: Understanding the factors and processes needed for modeling José Neira1*, Mauricio Ortiz1, Luis Morales2, and Edmundo Acevedo2 Oxygen is an important element for plant growth. Reducing its concentration in the soil affects plant physiological processes such as nutrient and water uptake as well as respiration, the redox potential of soil elements and the activity of microorganisms. The main mechanism of oxygen transport in the soil is by diffusion, a dynamic process greatly influenced by soil physical properties such as texture and structure, conditioning, pore size distribution, tortuosity and connectivity. Organic matter is a modifying agent of the soil’s chemical and physical properties, affecting its structure and the porous matrix, which are determinants of oxygen transport. This study reviews the theory of soil gas diffusion and the effect of soil organic matter on the soil’s physical properties and transport of gases. It also reviews gas diffusion models, particularly those including the effect of soil organic matter. Key words: Diffusion, diffusion coefficient, Fick’s laws, organic matter, oxygen transport. INTRODUCTION soil (Dp), which is a property of the medium and the gas under study and depends upon the texture, structure, Gas transport in the soil is a phenomenon in which gases distribution, size and connectivity of the pores as well as move mainly by diffusion. Diffusion is defined as the their tortuosity (Schjønning et al., 1999; Moldrup et al., random movement of particles due to kinetic energy; 2001). Compaction and water saturation of soils are the it may occur in a gaseous or liquid medium, with a net main barriers to soil oxygen transport, water being a more movement of the diffusing substance from a higher to effective barrier (Papendick and Runkles, 1965; Moldrup a lower concentration (Hillel, 2003). Gas diffusion is et al., 2000a; Neale et al., 2000). The diffusion of gases in conditioned by the physical properties of the soil, among water is slower than their diffusion in air by a factor of 104 which soil porosity is one of the most important. Soil (Call, 1957; Moldrup et al., 2000a; 2004; Thorbjørn et al., porosity is usually divided into the water-filled porosity 2008). (φ) and the air-filled porosity (ε) (Hillel, 1980), parameters The oxygen present in the atmosphere of the soil that have shown high correlation with plant production is used in different processes and may be limited by (Dasberg and Bakker, 1970). Larger pores generally allow flooding or by soil compaction, affecting plant growth more rapid movement of gases than smaller pores; thus, (Hillel, 2003; Lal and Shukla, 2004). There are three more gas diffusion occurs in the soil’s macropores (Horn conditions that relate soil oxygen concentration to plants. and Smucker, 2005), which are also used for root growth. In normoxia (normal conditions) respiration is aerobic, Therefore, it is expected that macropores will generally metabolism proceeds normally and most ATP is produced be well aerated and have higher oxygen concentrations, by oxidative phosphorylation. Under hypoxia oxygen while micropores will have a more deficient aeration. concentration begins to be limiting for ATP production Gases, including oxygen, move in the soil according by the oxidative phosphorylation pathway; while under to diffusion laws. The main parameter related to gas anoxia ATP is generated by glycolysis since no oxygen is diffusion in soil is the gas diffusion coefficient of the available (Saglio et al., 1988; Horchani et al., 2011). The effects of oxygen deficiency in the soil may be either direct or indirect; direct effects deal with the lack 1Centro de Estudios Avanzados en Fruticultura (CEAF), Camino Las of oxygen for plant processes, while indirect effects Parcelas 882, sector Los Choapinos, Rengo, Chile. are related to the physical and chemical properties of *Corresponding author ([email protected]). the soil that use oxygen (Lal and Shukla, 2004). Direct 2 Universidad de Chile, Facultad de Ciencias Agronómicas, Santa effects restrict processes such as plant respiration, water Rosa 11315, La Pintana, Santiago, Chile. Received: 14 January 2015. and nutrient absorption; they produce a change in root Accepted: 7 May 2015. metabolism towards fermentation. A critical and limiting doi:10.4067/S0718-58392015000300005 value of soil oxygen diffusion for crops is variable and CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 75 (Suppl. 1) AUGUST 2015 35 is called the oxygen diffusion rate or ODR (Glinski and The aim of this chapter is to discuss the theory of gas Stępniewski, 1985), which refers to the availability of diffusion, oriented in oxygen movement, and the soil oxygen for plants. It has been found that soil oxygen properties that affect the movement of oxygen in soil. -8 -2 -1 diffusion rates below 20 × 10 g O2 cm min do not permit plant emergence (Stolzy and Latey, 1964; Lal and THEORY OF GAS DIFFUSION IN THE SOIL Shukla, 2004). However, plants have the capability to adapt to a deficiency of oxygen in the soil by mechanisms Molecular gas diffusion in soils is controlled by the such as developing aerenchyma or by hormonal concentration gradient and the diffusion coefficient. adjustment (Armstrong et al., 1994). Mathematically, the movement of any gas in the soil under Indirect effects are produced when anaerobic conditions steady state conditions occurs according to the following in soil produce denitrification and reductions in some differential equation, which is Fick’s first law: elements such as Mn, Fe, and sulfate; indirect effects may be Q ∂c J = =D [1] divided into chemical and biological. At the chemical level, At p ∂x organic compounds from the decomposition of organic where J is the flux of a given gas, Q is the mass (g), A is 2 matter, such as ethylene, phenolic acids and acetic acid are the area (m ), t is time, Dp is the diffusion coefficient of produced, which are toxic to plants (Hillel, 2003; Lal and the gas in the soil, c is the concentration of the gas (g m-3) Shukla, 2004); low oxygen concentration also increases the and x is the distance. The processes that occur in the soil solubility of calcium carbonate, affecting the solubility of are more complex than those considered by Fick’s First Fe and inducing ferric chlorosis in trees. Manganese is also Law, since the flux of a gas in the soil varies over time; reduced in soils with poor aeration; when the reduced form that is, gas transport does not occur under steady state accumulates it generates toxic conditions for plants (Taylor conditions (Figure 1). Thus, the movement of oxygen in and Ashcroft, 1972). At the biological level a decrease in the soil is described by an equation applicable to transient oxygen produces anaerobic decomposition of soil organic conditions which also considers oxygen sources and matter (SOM), facilitating, for example, the generation of sinks: ammonia from protein decomposition instead of forming ∂c 2 =D ∂ c – S (Sx,t) [2] nitrates as would occur under normal conditions (Taylor ∂t p ∂x2 g and Ashcroft, 1972; Lal and Shukla, 2004). Figure 1. Scheme of soil oxygen dynamics. J is gas density flux, c is gas concentration (g m-3), t is time, x is distance, Sm is microorganism respiration, Sp is plant respiration, and Sr is redox reactions in the soil. 36 CHILEAN JOURNAL OF AGRICULTURAL RESEARCH 75 (Suppl. 1) AUGUST 2015 where c is gas concentration, t is time, x is distance system; thus, this soil property is sensitive to structural and Sg represents the consumption and/or evolution of changes (Bear, 1972; Dorner and Dec, 2007). Higher oxygen due to different sources (microorganisms, roots, values of soil permeability to air have been found in oxidation-reduction processes) and depends upon time structured compared to unstructured soils (McCarthy and and distance. Equation [2] has the following assumptions: Brown, 1992); thus, it is expected that soils with greater (1) Diffusion is the only mechanism for oxygen transport; air permeability will have larger gas diffusion coefficients convection is insignificant; and (2) macroscopic diffusion (Horn and Smucker, 2005). occurs in only one dimension. The soil oxygen diffusion is limited by two resistance The soil gas diffusion coefficient Dp incorporates factors related to soil structure and texture; the first is the effects of soil tortuosity and porosity; it is usually related to the blocking effect of water (w), indirectly estimated by the following equation: related to soil porosity, and the second is the effect of soil structural shape (p), directly related to soil particle size Dp = D0τε [3] 2 and tortuosity (Thorbjørn et al., 2008). Assuming that the where D0 is the diffusion coefficient of the gas in air (m s-1), ε is the soil air-filled porosity (m3 air m-3 soil) and τ soil pores are dry parallel tubes the two factors do not is the tortuosity of the soil. The soil porosity filled with limit oxygen diffusion and we can assume the oxygen flux air (ε) is a factor essentially controlled by the water-filled as free (Figure 2a). However, if we consider other soil porosity (φ) and the total porosity (Φ), which depend structural shapes, plus different water contents (Figures upon the soil type, organic matter, and management. The 2b-2c), a greater effect of p or w will be observed than in total soil porosity is mainly dependent on the texture and the simpler condition (Figure 2a). structure of the soil. Effect of SOM on the soil structure and on the soil EFFECT OF SOIL TEXTURE AND STRUCTURE oxygen diffusion ON GAS TRANSPORT The soil structure is the most important soil property related to oxygen diffusion in the soil, since oxygen The texture of a soil reflects the distribution of particle diffuses through the pore matrix.