Oecologia DOI 10.1007/s00442-015-3290-x
GLOBAL CHANGE ECOLOGY - ORIGINAL RESEARCH
The priming effect of soluble carbon inputs in organic and mineral soils from a temperate forest Hui Wang1,2 · Wenhua Xu1 · Guoqing Hu1,2 · Weiwei Dai1 · Ping Jiang1 · Edith Bai1
Received: 23 May 2014 / Accepted: 5 March 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract The priming effect (PE) is one of the most important interactions between C input and output in soils. Here we aim to quantify patterns of PE in response to six addition rates of 13C-labeled water-soluble C (WSC) and determine if these patterns are different between soil organic and mineral layers in a temperate forest. Isotope mass balance was used to distinguish WSC derived from SOC-derived CO2 respiration. The relative PE was 1.1–3.3 times stronger in the mineral layer than in the organic layer, indicating higher sensitivity of the mineral layer to WSC addition. However, the magnitude of cumulative PE was significantly higher in the organic layer than in the mineral layer due to higher SOC in the organic layer. With an increasing WSC addition rate, cumulative PE increased for both layers, but tended to level off when the addition rate was higher than 400 mg C kg−1 soil. This saturation effect indicates that stimulation of soil C loss by exogenous substrate would not be as drastic as the increase of C input. In fact, we found that the mineral layer with an WSC addition rate of 160–800 mg C kg−1 soil had net C storage although positive PE was observed. The addition of WSC basically caused net C loss in the organic layer due to the high magnitude of PE, pointing to the importance of the organic layer in C cycling of forest ecosystems. Our findings provide a fundamental understanding of PE on SOC Communicated by Hormoz BassiriRad. * Edith Bai [email protected] 1
State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China
2
College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China
mineralization of forest soils and warrant further in situ studies of PE in order to better understand C cycling under global climate change. Keywords Soil organic carbon mineralization · Substrate availability · Nutrient status · Microbial biomass · Carbon sequestration
Introduction Soil organic C (SOC) is the largest C pool in terrestrial ecosystems, and stores three times as much C as in the atmosphere or in plant biomass (Schmidt et al. 2011). The CO2 efflux from the soil to the atmosphere is 98 ± 12 Pg C year−1, about ten times greater than that from fossil fuel combustion and deforestation combined (Bond-Lamberty and Thomson 2010), which means that small changes in soil C dynamics may induce a significant increase of the atmospheric CO2 concentration. With increasing atmospheric CO2 concentration and temperature, the input of exogenous substrate to soil via plant residue or root exudation might increase (Cheng 1999; Raich et al. 2006). Moreover, soil has many microbial hotspots which receive a high input rate of exogenous C, such as the rhizosphere, detritusphere, drillosphere and some other biopores (Kuzyakov 2010). Thus, understanding the relationship between substrate input rate and soil organic matter (SOM) decomposition is essential for better prediction of soil C dynamics under global climate change. Most process-based models consider SOM decomposition a function of first-order rate constants (Jenkinson and Coleman 2008; Manzoni and Porporato 2009). However, interactions between C input and output such as the priming effect (PE), defined as changes in SOM decomposition
13
Oecologia
Soil properties Microbial biomass & microbial community DOC and SOC content Nutrient status
Other soil properties such as aggregate, texture, pH, moisture, etc.
Exogenous substrate properties Substrate quantity Substrate quality
Priming effect
Fig. 1 Conceptual diagram of factors influencing the priming effect (PE). Both exogenous substrate properties and soil properties could affect the PE. Solid lines represent direct effects and dashed lines represent indirect effects. DOC Dissolved organic C, SOC soil organic C
after the inputs of exogenous substrate (Kuzyakov et al. 2000), have been suggested as crucial mechanisms which need to be incorporated into future ecosystem models (Cheng et al. 2014). One of the most important reasons for not taking PE into consideration in most C cycling models is its variability and unpredictability (Paterson and Sim 2013). Quantitative relationships between the magnitude of PE and the substrate addition rate have been found in recent studies (Blagodatskaya and Kuzyakov 2008; Guenet et al. 2010; Paterson and Sim 2013), all of which showed a nonlinear response of PE to the substrate addition rate, indicating that the ratio of PE to substrate addition rate always decreases with an increasing amount of exogenous substrate. However, using the substrate input rate as a predictor of PE is far from practical application in models because this relationship might be variable for different soils (De Graaff et al. 2014; Salomé et al. 2010). A prevalent view is that PE is driven by exogenous substrates, but may be mediated by soil properties such as microbial characteristics, nutrient status, and SOC content (Fig. 1) (Chen et al. 2014; Chowdhury et al. 2014; Fontaine et al. 2011; Sullivan and Hart 2013). Addition of exogenous substrates could affect PE through changing soil microbial characteristics (Fig. 1). In addition, other soil properties such as soil texture and aggregate, soil pH, and soil moisture could affect PE indirectly (Fig. 1) (Blagodatskaya and Kuzyakov 2008; Sullivan and Hart 2013). Among those factors affecting PE, the impact of nutrient availability has recently been widely studied (Chen et al. 2014; Chowdhury et al. 2014; Fontaine et al. 2011; Sullivan and Hart 2013). While soil microbial growth is stimulated by exogenous C addition, other nutrients such as N could become limiting, causing nutrient mining from SOM by microbes, and thereby a positive PE (the nutrient mining
13
theory) (Blagodatskaya and Kuzyakov 2008; Fontaine et al. 2003). Therefore, soil with higher nutrient availability is expected to have lower PE. However, contrasting results have been found (Chen et al. 2014; Chowdhury et al. 2014), which may be partly due to the interactions between soil C and N availability (Craine et al. 2007). The degree of nutrient limitation of SOM mineralization has been found to increase with depth through the soil profile (Fierer et al. 2003). In boreal or temperate forests, the organic layer has a higher SOC content and could provide more C sources for priming, but the mineral layer might be more susceptible to exogenous substrate input according to the nutrient mining theory. Therefore, study of the differences between these two layers provides an opportunity to explore how exogenous substrate input and soil properties interact to affect PE. Until now, comparative studies of PE in organic and mineral layers are scarce and the only existing result, of stronger PE in topsoil than subsoil, still needs to be tested because forest soils have never been studied with regard to this (De Graaff et al. 2014; Paterson and Sim 2013). The objectives of our study were to quantify the pattern of PE in response to water-soluble C (WSC) (extracted from birch leaves) addition, and to determine if this pattern is different between soil organic and mineral layers in a temperate old-growth broadleaf and mixed Korean pine forest. Isotope labeling was used to distinguish WSC derived from SOC-derived respired CO2, soil microbial biomass C (MBC) and dissolved organic C (DOC) during the 53-day incubation. We hypothesized that: 1. A higher WSC supply should cause a higher PE on SOM mineralization because more soil microorganisms are stimulated by labile C, inducing higher SOM mineralization. However, the relationship between WSC addition rate and PE may not be linear considering substrate saturation for soil microbes. 2. The mineral layer with lower N availability should be more sensitive to exogenous substrate addition (i.e., higher relative PE) according to the nutrient mining theory.
Materials and methods Site, soils and 13C‑enriched WSC The study site is located int an old-growth broadleaf and mixed Korean pine forest in Mountain Changbai, Northeast China (42°23′N, 128°05′E and 800 m a.s.l.). Mean annual precipitation is 700 mm, mean annual temperature is 3.0 °C, and Pinus koraiensis, Tilia amurensis, Quercus mongolica, Betula platyphylla, Fraxinus mandshurica and Acer mono
Oecologia Table 1 Main characteristics of the studied organic layer and mineral layer soils of the temperate forest ecosystem
Organic layer
Mineral layer
14.98 (0.18)a 0.90 (0.09)a 16.62 (0.03)a −28.02 (0.01)a 5.26 (0.23)a 102.14 (7.70)a
1.52 (0.07)b 0.12 (0.01)b 12.85 (0.59)b −27.46 (0.09)a 5.13 (0.15)a 39.86 (2.12)b
Soil organic C (SOC) (%) Total N (TN) (%) C/N ratio Stable C isotope ratio (δ13C) (‰) pH (H2O) Water-holding capacity (WHC) (%) Particle size fraction (%) Clay (2,000 μm)a Small macroaggregate (250–2,000 μm) Microaggregate (53–250 μm) Silt plus clay particles (
GLOBAL CHANGE ECOLOGY - ORIGINAL RESEARCH
The priming effect of soluble carbon inputs in organic and mineral soils from a temperate forest Hui Wang1,2 · Wenhua Xu1 · Guoqing Hu1,2 · Weiwei Dai1 · Ping Jiang1 · Edith Bai1
Received: 23 May 2014 / Accepted: 5 March 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract The priming effect (PE) is one of the most important interactions between C input and output in soils. Here we aim to quantify patterns of PE in response to six addition rates of 13C-labeled water-soluble C (WSC) and determine if these patterns are different between soil organic and mineral layers in a temperate forest. Isotope mass balance was used to distinguish WSC derived from SOC-derived CO2 respiration. The relative PE was 1.1–3.3 times stronger in the mineral layer than in the organic layer, indicating higher sensitivity of the mineral layer to WSC addition. However, the magnitude of cumulative PE was significantly higher in the organic layer than in the mineral layer due to higher SOC in the organic layer. With an increasing WSC addition rate, cumulative PE increased for both layers, but tended to level off when the addition rate was higher than 400 mg C kg−1 soil. This saturation effect indicates that stimulation of soil C loss by exogenous substrate would not be as drastic as the increase of C input. In fact, we found that the mineral layer with an WSC addition rate of 160–800 mg C kg−1 soil had net C storage although positive PE was observed. The addition of WSC basically caused net C loss in the organic layer due to the high magnitude of PE, pointing to the importance of the organic layer in C cycling of forest ecosystems. Our findings provide a fundamental understanding of PE on SOC Communicated by Hormoz BassiriRad. * Edith Bai [email protected] 1
State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China
2
College of Resources and Environment, University of Chinese Academy of Sciences, Beijing 100049, China
mineralization of forest soils and warrant further in situ studies of PE in order to better understand C cycling under global climate change. Keywords Soil organic carbon mineralization · Substrate availability · Nutrient status · Microbial biomass · Carbon sequestration
Introduction Soil organic C (SOC) is the largest C pool in terrestrial ecosystems, and stores three times as much C as in the atmosphere or in plant biomass (Schmidt et al. 2011). The CO2 efflux from the soil to the atmosphere is 98 ± 12 Pg C year−1, about ten times greater than that from fossil fuel combustion and deforestation combined (Bond-Lamberty and Thomson 2010), which means that small changes in soil C dynamics may induce a significant increase of the atmospheric CO2 concentration. With increasing atmospheric CO2 concentration and temperature, the input of exogenous substrate to soil via plant residue or root exudation might increase (Cheng 1999; Raich et al. 2006). Moreover, soil has many microbial hotspots which receive a high input rate of exogenous C, such as the rhizosphere, detritusphere, drillosphere and some other biopores (Kuzyakov 2010). Thus, understanding the relationship between substrate input rate and soil organic matter (SOM) decomposition is essential for better prediction of soil C dynamics under global climate change. Most process-based models consider SOM decomposition a function of first-order rate constants (Jenkinson and Coleman 2008; Manzoni and Porporato 2009). However, interactions between C input and output such as the priming effect (PE), defined as changes in SOM decomposition
13
Oecologia
Soil properties Microbial biomass & microbial community DOC and SOC content Nutrient status
Other soil properties such as aggregate, texture, pH, moisture, etc.
Exogenous substrate properties Substrate quantity Substrate quality
Priming effect
Fig. 1 Conceptual diagram of factors influencing the priming effect (PE). Both exogenous substrate properties and soil properties could affect the PE. Solid lines represent direct effects and dashed lines represent indirect effects. DOC Dissolved organic C, SOC soil organic C
after the inputs of exogenous substrate (Kuzyakov et al. 2000), have been suggested as crucial mechanisms which need to be incorporated into future ecosystem models (Cheng et al. 2014). One of the most important reasons for not taking PE into consideration in most C cycling models is its variability and unpredictability (Paterson and Sim 2013). Quantitative relationships between the magnitude of PE and the substrate addition rate have been found in recent studies (Blagodatskaya and Kuzyakov 2008; Guenet et al. 2010; Paterson and Sim 2013), all of which showed a nonlinear response of PE to the substrate addition rate, indicating that the ratio of PE to substrate addition rate always decreases with an increasing amount of exogenous substrate. However, using the substrate input rate as a predictor of PE is far from practical application in models because this relationship might be variable for different soils (De Graaff et al. 2014; Salomé et al. 2010). A prevalent view is that PE is driven by exogenous substrates, but may be mediated by soil properties such as microbial characteristics, nutrient status, and SOC content (Fig. 1) (Chen et al. 2014; Chowdhury et al. 2014; Fontaine et al. 2011; Sullivan and Hart 2013). Addition of exogenous substrates could affect PE through changing soil microbial characteristics (Fig. 1). In addition, other soil properties such as soil texture and aggregate, soil pH, and soil moisture could affect PE indirectly (Fig. 1) (Blagodatskaya and Kuzyakov 2008; Sullivan and Hart 2013). Among those factors affecting PE, the impact of nutrient availability has recently been widely studied (Chen et al. 2014; Chowdhury et al. 2014; Fontaine et al. 2011; Sullivan and Hart 2013). While soil microbial growth is stimulated by exogenous C addition, other nutrients such as N could become limiting, causing nutrient mining from SOM by microbes, and thereby a positive PE (the nutrient mining
13
theory) (Blagodatskaya and Kuzyakov 2008; Fontaine et al. 2003). Therefore, soil with higher nutrient availability is expected to have lower PE. However, contrasting results have been found (Chen et al. 2014; Chowdhury et al. 2014), which may be partly due to the interactions between soil C and N availability (Craine et al. 2007). The degree of nutrient limitation of SOM mineralization has been found to increase with depth through the soil profile (Fierer et al. 2003). In boreal or temperate forests, the organic layer has a higher SOC content and could provide more C sources for priming, but the mineral layer might be more susceptible to exogenous substrate input according to the nutrient mining theory. Therefore, study of the differences between these two layers provides an opportunity to explore how exogenous substrate input and soil properties interact to affect PE. Until now, comparative studies of PE in organic and mineral layers are scarce and the only existing result, of stronger PE in topsoil than subsoil, still needs to be tested because forest soils have never been studied with regard to this (De Graaff et al. 2014; Paterson and Sim 2013). The objectives of our study were to quantify the pattern of PE in response to water-soluble C (WSC) (extracted from birch leaves) addition, and to determine if this pattern is different between soil organic and mineral layers in a temperate old-growth broadleaf and mixed Korean pine forest. Isotope labeling was used to distinguish WSC derived from SOC-derived respired CO2, soil microbial biomass C (MBC) and dissolved organic C (DOC) during the 53-day incubation. We hypothesized that: 1. A higher WSC supply should cause a higher PE on SOM mineralization because more soil microorganisms are stimulated by labile C, inducing higher SOM mineralization. However, the relationship between WSC addition rate and PE may not be linear considering substrate saturation for soil microbes. 2. The mineral layer with lower N availability should be more sensitive to exogenous substrate addition (i.e., higher relative PE) according to the nutrient mining theory.
Materials and methods Site, soils and 13C‑enriched WSC The study site is located int an old-growth broadleaf and mixed Korean pine forest in Mountain Changbai, Northeast China (42°23′N, 128°05′E and 800 m a.s.l.). Mean annual precipitation is 700 mm, mean annual temperature is 3.0 °C, and Pinus koraiensis, Tilia amurensis, Quercus mongolica, Betula platyphylla, Fraxinus mandshurica and Acer mono
Oecologia Table 1 Main characteristics of the studied organic layer and mineral layer soils of the temperate forest ecosystem
Organic layer
Mineral layer
14.98 (0.18)a 0.90 (0.09)a 16.62 (0.03)a −28.02 (0.01)a 5.26 (0.23)a 102.14 (7.70)a
1.52 (0.07)b 0.12 (0.01)b 12.85 (0.59)b −27.46 (0.09)a 5.13 (0.15)a 39.86 (2.12)b
Soil organic C (SOC) (%) Total N (TN) (%) C/N ratio Stable C isotope ratio (δ13C) (‰) pH (H2O) Water-holding capacity (WHC) (%) Particle size fraction (%) Clay (2,000 μm)a Small macroaggregate (250–2,000 μm) Microaggregate (53–250 μm) Silt plus clay particles (
