The afterlife effects of leaf and root litter traits on soil N cycling

Abstract

1 INTRODUCTION

Nitrogen (N) is the dominant element in the Earth's atmosphere, and an important constituent of the biosphere, yet it often limits ecosystem productivity owing to its near-absence in bedrock (LeBauer & Treseder, 2008). The availability of N to plants is mainly controlled by organic matter decomposition, during which organic N is immobilized as it becomes incorporated in microbial biomass, or mineralized, that is converted into inorganic forms (Figure 1). The inorganic N content in the soil solution is strongly determined by the rate of net N mineralization (Li et al., 2019; Schimel & Bennett, 2004), that is when mineralized N exceeds microbial demand. It is also important for ecosystem productivity as inorganic N is the predominant source of N for plants.

FIGURE 1

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Schematic overview of pools and fluxes related to N dynamics during decomposition. Inspired by Geisseler et al. (2010), Averill and Waring (2018), Cotrufo et al. (2021), Jilling et al. (2018) and Zhang et al. (2021).

The rate and temporal dynamics of N mineralization and release in the soil solution, and its incorporation into soil fractions are of fundamental importance for plant growth and ecosystem productivity. Yet, our knowledge of how litter decomposition drives N dynamics and affects the fate of N in the soil is still rather limited. Nitrogen dynamics during decomposition in soils are affected by various abiotic (e.g. soil properties; Villarino et al., 2023) and biotic (e.g. rhizodeposition; Berenstecher et al., 2023; Jilling et al., 2018) parameters. Yet, multiple studies have shown that initial litter chemistry may be the predominant influence on N dynamics during decomposition and eventually on the quantity of inorganic N in the soil solution (Chen et al., 2015; Orwin et al., 2010; Trinsoutrot, Recous, Bentz, et al., 2000; Trinsoutrot, Recous, Mary, et al., 2000; van Huysen et al., 2013). As such, ample evidence exists that the initial litter N concentration and the C/N ratio strongly affect litter net N release, that is the loss of N measured by changes in litter N concentration (Kriiska et al., 2021; Manzoni et al., 2008; Moore et al., 2011; Parton et al., 2007; Pei et al., 2019; van Huysen et al., 2013). Litters with a relatively high C/N ratio, which may reinforce microbial N limitation, often lead to net N immobilization during the initial stages of decomposition, contrary to litters with a relatively low C/N ratio that favour net N mineralization (Trinsoutrot, Recous, Bentz, et al., 2000). Yet, the litter C/N is not always the main determinant of the net release of inorganic N into the soil solution (Chen et al., 2014).

In particular, it has also been observed that high initial litter cellulose concentrations may promote net N mineralization (Chen et al., 2015), while high initial litter lignin (van Huysen et al., 2013) and polyphenol concentrations (Fernández-Alonso et al., 2018; Oglesby & Fownes, 1992; Trinsoutrot, Recous, Bentz, et al., 2000) appear to retard N mineralization. Tannins are known to form complexes with proteins and thereby inhibit N mineralization (Schimel et al., 1998) and nitrification (Baldwin et al., 1983). Large amounts of phenolic compounds have also been shown to accelerate bulk litter mass loss when C availability rather than N availability primarily limits microbial decomposers (Hättenschwiler & Jørgensen, 2010). Other litter traits, such as calcium (Ca) (Hobbie, 2015), manganese (Mn) and magnesium (Mg) concentrations (Vivanco & Austin, 2019) could also play an important role in decomposition and N cycling. Ca and Mg are important base cations that may accelerate initial decomposition (Aponte et al., 2013; García-Palacios et al., 2016), potentially leading to faster N release from litter. Mn may be significant for the degradation of lignin (Keiluweit et al., 2015) with positive consequences for the release of N from formerly shielded N compounds.

During organic matter decomposition, N contained in free particulate organic matter (POM, which is a heterogeneous pool of small litter fragments, litter decomposition by-products and soil OM not associated with minerals) can be incorporated into soil aggregates (i.e. aggregated POM), which typically confers only a moderate protection from microbial degradation (Lavallee et al., 2020; von Lützow et al., 2006). Stronger protection is provided when both organic and inorganic N are immobilized by being sorbed onto minerals or by forming interactions with organo-mineral complexes, thereby becoming part of the mineral-associated OM (MAOM) fraction (Hatton et al., 2012; Hatton, Remusat, et al., 2015; Poirier et al., 2014; von Lützow et al., 2006). In contrast to POM, which typically represents a more labile fraction with a shorter residence time, MAOM is more stable, serving as a key component in nutrient storage and slow-release processes over time (Lavallee et al., 2020).

Litter quality may also be an important control of the N stabilized in MAOM (Angst et al., 2021; Córdova et al., 2018). According to the Microbial Efficiency-Matrix Stabilization (MEMS) framework (Cotrufo et al., 2013), a higher initial litter quality (e.g. a higher N concentration and labile C compounds content) may promote the stabilization of SOM via the microbial pathway (Angst et al., 2019; Cyle et al., 2016; Hatton, Castanha, et al., 2015; Liang et al., 2019) through a higher production of microbial-derived products, which may eventually be stabilized as MAOM (Cotrufo et al., 2013). However, opposite effects of litter quality on the stabilization of SOM have also been reported. As such, several studies found that less MAOM was stabilized by high-quality litters. Suggested underlying mechanisms included soil C saturation (Castellano et al., 2015; Huys et al., 2022), higher C mineralization rates of high-quality litters (Córdova et al., 2018), or the role of fungi, whose growth may be promoted by low-quality litters, in MAOM formation (Zheng et al., 2021). Another study observed that the addition of low C/N (i.e. high quality) material induced a positive priming effect, and thus stimulated the breakdown of SOM (Mason-Jones et al., 2018). These observations question the generality of the MEMS framework. While the vast majority of studies related to MAOM and POM formation during decomposition have focused on C, understanding the determinant of N stabilized in MAOM-N and in POM-N has largely been understudied despite its crucial importance for our understanding of the N cycle (but see Jilling et al., 2018).

Most of these previous studies focused on leaf litter only, although fine-root litter represents another major source of N to the soil (Freschet et al., 2013) and may more strongly affect SOM dynamics (Kyaschenko et al., 2019). Leaf and fine-root litter can greatly differ in their initial chemical composition, that is such as in initial N concentrations (e.g. Song et al., 2021), and fine-root litter is more intimately in contact with the soil matrix. Consequently, litter N release patterns associated with their decomposition (Fornara et al., 2009; Moretto et al., 2001; Parton et al., 2007) and N availability to plants (Bird et al., 2008; Hatton, Castanha, et al., 2015) may also vary between root and leaf litter types.

In contrast to C dynamics, which follow the same pattern as litter mass loss during decomposition, N dynamics can differ considerably (Lindahl et al., 2007; Xiong et al., 2013). Typically, N release patterns are characterized by three phases: an initial phase dominated by N leaching, followed by a phase of immobilization where N concentration in the decomposing litter increases, and finally, a phase of continuous release of N (Ball et al., 2009). These phases and the timing of N release can vary greatly depending on initial litter quality (Parton et al., 2007). Manzoni et al. (2010) suggested that the initial C/N ratio is among the most important determinant of the N release patterns. The relative importance of initial litter traits for N dynamics can vary during the different decomposition stages. For example, higher initial litter N concentrations may accelerate decomposition and N release during early-stage decomposition, while it can have the opposite effect (Hobbie, 2015) or no effect during later stages, when lignin concentration may be the primary control (Oglesby & Fownes, 1992; Pei et al., 2019). Most studies have focused on the early stages of litter decomposition and, more importantly, have not quantified the fate of the N released from litter in the soil. Furthermore, it remains unclear whether and how leaf and fine-root litter differ in N release dynamics under the influence of different litter traits.

With this study, we compared litter N release dynamics and the fate of N within the soil between leaf and fine-root litter from 12 plant species using a stable isotope approach. Indeed, the labelling of litter with the stable isotope ¹⁵N allows more detailed insight into N transformation processes during decomposition (Zeller et al., 2000, 2001) and how it impacts N availability in the soil solution (Schimel & Bennett, 2004).

We hypothesized that:

1. During leaf and fine-root litter decomposition, litter N release and the availability of soil inorganic N increase with increasing initial litter N and decreasing initial litter C/N.
2. Beyond initial N and C/N, high concentrations in other litter nutrients such as Ca, Mg and Mn positively affect litter N release and soil inorganic N accumulation during early stages of decomposition. In contrast, higher initial concentrations of lignin negatively affect litter N release and soil inorganic N accumulation during later stages of decomposition.
3. High litter N release is linked to less N in the POM pool and more N stabilized in the MAOM pool.
4. The overall distinct trait syndrome of leaf vs. fine-root litter results in different N dynamics and fates during decomposition. Leaf litter generally releases N faster, contributes more N to the soil solution during early-stage decomposition and leads to a higher proportion of N in the MAOM-N soil fraction compared to fine-root litter.