Soil fauna show different degradation patterns of lignin and cellulose along an elevational gradient

Highlights

• Warmer temperatures accelerated cellulose and lignin degradation independently of litter type

• Stimulating effects of fauna on cellulose and lignin degradation consistently occurred after 156–277 days of decomposition

• Soil faunal contributions to cellulose and lignin decomposition were 11.7–34.2 % and 14.2–32.7 %, respectively

• Temperature and fauna abundance positively affected the faunal effects on cellulose and lignin degradation

Abstract

The degradations of Cellulose and lignin from litter are crucial processes for carbon and nutrient cycling in forest ecosystems. However, the effects of soil fauna on these degradation processes are unclear despite their functional roles in litter fragmentation and microorganism regulation. Here we conducted a four-year field experiment using litterbags with two mesh sizes (3 and 0.04 mm) to assess the effects of soil fauna on cellulose and lignin degradation at four different elevations in southwestern China. Our results showed that the remaining masses of cellulose and lignin increased with elevation in the both meshed litterbags. Soil fauna decreased the remaining cellulose and lignin masses after 156–277 days of decomposition. At the end of the experiment, the stimulating effects of the soil fauna on the cellulose and lignin degradation were 11.7–34.2% and 14.2–32.7%, respectively, while soil fauna effects differed in magnitude on the degradations of lignin (higher) and cellulose (lower). The effects of soil fauna on lignin degradation significantly increased as the elevation decreased, regardless of the litter type; whereas soil fauna-derived cellulose degradation did not show the same pattern. The increases in temperature and/or fauna abundance promoted the effects of soil fauna on cellulose and lignin degradation, and these fauna effects were dependent to litter quality. These findings highlight that soil fauna promote cellulose and lignin degradation in different magnitude and these degradations are largely dependent on climate conditions and litter types.

Introduction

Plant litter decomposition is critical for the cycling of soil organic matter in terrestrial ecosystems (Aerts, 1997; Berg, 2000). Climate, litter quality and the decomposer community (arranged according to decrease in importance) are thought to be the primary drivers of litter decomposition rates (Cornwell et al., 2008; Bradford et al., 2016; Yin et al., 2019). Lignin and cellulose are the most abundant components of plant litter and account for >50% of the carbon sequestered in plant materials (Boerjan et al., 2003; Kalbitz et al., 2006; Rahman et al., 2013). Previous studies have suggested that the degradation of lignin and cellulose had important implications for litter decomposition rates (Fioretto et al., 2005; Kalbitz et al., 2006; Klotzbücher et al., 2011). Furthermore, the biodegradation of these recalcitrant components is tightly linked to soil fauna and microorganism interactions in detritus food chains (Pérez et al., 2002; Klotzbücher et al., 2011). The feeding activity, community biomass, population size, body size, species richness and functional composition of soil fauna have been considered to affect the patterns of litter lignin and cellulose decomposition (Bradford et al., 2002; Hättenschwiler and Gasser, 2005; Wall et al., 2008; Frouz, 2018).

Soil fauna can accelerate organic matter mineralization and nutrient cycling directly by digesting and fragmenting litter and indirectly by altering the soil structure, litter surfaces and the composition of microbial community (González and Seastedt, 2001; Bradford et al., 2002; Huhta, 2007; Yin et al., 2019). Numerous results have demonstrated that the effects of soil fauna on decomposition rates are dependent on the prevailing climatic conditions, and greater fauna effects generally occur at low elevation and latitude sites due to the higher abundance and diversity of soil fauna in warmer and wetter climatic conditions (García-Palacios et al., 2013; Liao et al., 2016; Wang et al., 2018). Moreover, variations in litter lignin and cellulose concentrations during the early stage of decomposition can alter the later stage of decomposition and even the pattern of whole decomposition process (Fioretto et al., 2005; Rahman et al., 2013; Yue et al., 2016), and changes in the litter lignin concentration are also a predominant regulator of the decomposer community composition and decomposition rates (Pérez et al., 2002; Wang et al., 2018). Furthermore, the community composition of soil fauna is sensitive to the heterogeneity of litter quality across different climatic conditions (Makkonen et al., 2012; García-Palacios et al., 2013). High-quality litter (i.e., low ratios of C:N, lignin:N and lignin:cellulose) facilitates the consumption and colonization of soil invertebrate communities during litter decomposition (Makkonen et al., 2012; He et al., 2015, He et al., 2016; Wang et al., 2018). However, little information is available on how soil fauna control the processes of lignin and cellulose degradation during litter decomposition within and among ecosystems.

In general, it is thought that cellulose provides the dominant source of C in the early stages of decomposition (Fioretto et al., 2005; Berg and McClaugherty, 2014; He et al., 2015), and the decomposition of cellulose is relatively fast because its relatively simple structure (a long chain of glucose molecules) can be decomposed more easily by soil fauna and various microorganisms (Brown et al., 1967; Pérez et al., 2002; Wu, 2018). In contrast, lignin is thought to affect the mass loss in the late stages of decomposition (Fioretto et al., 2005; He et al., 2016), and lignin is more difficult for soil organisms to decompose since it has a stable and complex structure (a three-dimensional macromolecule). Only specialized fauna (termites) and microorganisms (mainly Basidiomycetes) are able to synthesize extracellular enzymes that are capable of metabolizing the recalcitrant lignin molecules into biologically accessible forms (Rahman et al., 2013; Yue et al., 2016; Frouz, 2018). Furthermore, cellulose is known to be protected by lignin in plant cell walls, which prevents the cellulose from enzymatic hydrolysis (Berg and McClaugherty, 2014; Keiser and Bradford, 2017). Thus, the differences in molecular structure between cellulose and lignin exert an important effect on the decomposition patterns (Fioretto et al., 2005). In addition, litter species have been regarded as a predominant factor affecting litter decomposition, and the rates of lignin and cellulose degradation can change significantly among different litter species (Cornwell et al., 2008; García-Palacios et al., 2013; Bradford et al., 2016). Therefore, the effects of soil fauna on lignin and cellulose degradation might differ significantly at different decomposition stages and in different forest ecosystems (Keiser and Bradford, 2017; Wang et al., 2018). Nevertheless, few studies have addressed the effects of soil fauna on lignin and cellulose degradation during litter decomposition along an elevational gradient.

The regions between the eastern Tibetan Plateau and Sichuan Basin have an obvious elevational gradient from 400 m to 4500 m a.s.l. (Liu et al., 2019; Tan et al., 2019), which leads to significant variations in climate, plant vegetation and the decomposer community (Tan et al., 2013a, Tan et al., 2013b; Tan et al., 2019). Therefore, a four-year field experiment was conducted using litterbags with two mesh sizes (3 and 0.04 mm) to assess the fauna effects on litter decomposition at 4 different elevations. The total difference in elevation between our forest study sites was 3100 m a.s.l. We aimed to quantify the activities of the soil fauna on cellulose and lignin degradation in different subtropical forests. Specifically, we hypothesized that: (1) the fauna effects on cellulose and lignin degradation would decrease from the lower to higher elevations since the lower temperatures found at higher elevations would constrain the abundance of the soil fauna and their activity and (2) higher fauna effects on cellulose and lignin degradation would occur in litter species with low-quality (e.g., high lignin content and lignin/N) because the degradation of the recalcitrant component in these litter species is more associated with the fauna-microbe interaction.