Author contributions:
Junbo Yang: Conceptualization (equal); Data Curation (equal); Formal analysis (equal); Investigation (equal); Methodology (equal); Visualization (equal); Writing - Original Draft Preparation (equal); Writing - Review & Editing (equal);
Kai Tian: Conceptualization (equal); Investigation (equal); Methodology (equal); Software (equal); Writing - Review & Editing (equal);
Jingzhong Lu: Conceptualization (equal); Methodology (equal); Software (equal); Visualization (equal); Writing - Review & Editing (equal);
Xiangshi Kong: Investigation (equal); Validation (equal); Writing - Review & Editing (equal);
Qiang Li: Investigation (equal); Validation (equal); Writing - Review & Editing (equal);
Rumeng Ye: Investigation (equal); Validation (equal);
Xiaoyi Zeng: Investigation (equal); Validation (equal); Writing - Review & Editing (equal);
Tingting Cao: Investigation (equal); Validation (equal); Writing - Review & Editing (equal);
Haijing Hu: Investigation (equal); Validation (equal);
Yanli Ji: Investigation (equal); Validation (equal);
Xingjun Tian: Conceptualization (equal); Data Curation (equal); Funding acquisition (equal); Project Administration (equal); Resources (equal); Supervision (equal); Writing - Review & Editing (equal);
Stefan Scheu: Conceptualization (equal); Writing - Review & Editing (equal).
Earthworms increase forest litter mass loss irrespective of deposited compounds – A field manipulation experiment in subtropical forests
Abstract
Earthworms modulate the carbon and nitrogen cycling in terrestrial ecosystems, their effect may be affected by deposited compounds due to human activity such as industrial emissions. However, studies investigating how deposited compounds affect the role of earthworms in carbon cycling such as litter decomposition are lacking, although they are important for understanding the influence of deposited compounds on ecosystems and the bioremediation by applying earthworms. For this, we performed a 365-day in situ litterbag decomposition experiment in a deciduous (Quercus variabilis ) and coniferous (Pinus massoniana ) forest in southeast China. We manipulated nitrogen (N), sodium (Na) and polycyclic aromatic hydrocarbon (PAH) deposited compounds during litter decomposition with and without earthworms (Eisenia fetida ). After one year, N, Na and PAH compounds all slowed down litter mass loss, with the effects of Na being the strongest. By contrast, E. fetida generally increased litter mass loss and their positive effects were uniformly maintained irrespective of the type of deposited compounds. Further, the pathways earthworms increasing litter mass loss varied among the types of deposited compounds and forests. As indicated by structural equation modeling, earthworms maintained their positive effects and mitigated the negative effects of deposited compounds by directly increasing litter mass loss and indirectly increasing soil pH and microbial biomass. Overall, the results indicate that the acceleration of earthworms on litter mass loss is not affected by deposited compounds, with the pathways of earthworms increasing litter mass loss varying among the types of deposited compounds and forests. This suggests that the effects of atmospheric deposited compounds and earthworms on terrestrial ecosystem processes need to be taken into account because earthworms may cancel out the detrimental influence of deposited compounds on litter decomposition.
Keywords : Aboveground–belowground linkages, Carbon cycling, Brown food web, Eisenia fetida , Atmospheric depositions, Subtropic forests
1 Introduction
Human activities such as industrial emissions increase the inputting of atmospheric deposited compounds to natural ecosystems, these compounds affect major process of carbon cycling such as litter decomposition (Knorr et al., 2005). In terrestrial ecosystems, litter decomposition is accelerated by soil decomposers such as soil engineers, earthworms (Cortez, 1998). Although the effects of deposited compounds and earthworms on litter decomposition were studied separately, their interactive effect remains elusive (Zhang et al., 2018; Huang et al., 2020). However, this gap limits our understanding of the influence of deposited compounds on terrestrial ecosystems and the role of earthworms under the increasing input of deposited compounds. In addition, filling this gap is important for bioremediation, e.g., applying earthworms to forests contaminated by industrial emissions.
Earthworms as major soil detritivores form part of the soil macrofauna, they have been suggested to contribute to litter decomposition by directly fragmenting litter and indirectly influencing soil properties, and the structure and activities of both microbes and fauna (Schulmann and Tiunov, 1999; Kizilkaya et al., 2011; Sackett et al., 2013).Eisenia fetida was found abundant in compost heaps where it accelerates organic matter decomposition (Aira et al., 2006). However,E. fetida also lives in natural forests in southern Europe and eastern China, in particular close to urban areas (Huang et al., 2003). This epigeic species predominantly colonizes in the litter layer, and able to live in contaminated sites (Rodriguez-Campos et al., 2014). Whereas, how the effect of E. fetida on forest litter decomposition varied with different deposited compounds received little attention, this is a very essential work to explore the application method of using epigeic earthworms for the bioremediation of contaminated forest soils.
Atmospheric depositions are changing terrestrial ecosystems at global scales (Holland et al., 2005; Liu et al., 2011). In particular, human activities such as industrial emissions are leading to increase the input of different deposited compounds into forests soil, e.g., ammonium (N), sodium (metal ions Na) and polycyclic aromatic hydrocarbons (organic contaminant PAHs) (Wang et al., 2015; Li et al., 2016). In the forests near urban regions, artificial road salt in winter may also increase the Na content in soil (Tiwari & Rachlin, 2018). Although three deposited compounds are generally at relatively low rates in natural conditions, each of them has been shown to affect litter mass loss by influencing soil microbial, faunal decomposer and the habitat of these decomposers (Knorr et al., 2005; Qasemian et al., 2012; Kaspari et al., 2014). Especially, these deposited compounds at high concentrations may detrimentally affect litter mass loss (Liu et al., 2011; Zhang et al., 2016). In addition, the effects of the three deposited compounds during litter mass loss may be different based on their specific chemical properties. For example, N addition may promote soil acidification but affect effect of soil fauna little (Zhang et al., 2016; Lin et al., 2017); Na addition may meet the Na shortage of soil fauna but prohibit microbial activities in inland forests (Kaspari et al., 2014; Jia et al., 2015); PAHs are toxic to soil microbial and faunal decomposers (Cotrufo et al., 2014; Klamerus-Iwan et al., 2015). Although the effects of N, Na and PAHs on litter mass loss were well studied separately (Knorr et al., 2005; Qasemian et al., 2012; Kaspari et al., 2014), their effects on litter mass loss have not been investigated in concert with earthworms in forests. This, however, is important for understanding the interactive effects of deposited compounds and soil keystone species on nutrient cycling in terrestrial ecosystems.
Here, we explored how the effects of earthworms on litter mass loss interactive with atmospheric deposited compounds including N, Na and PAHs. We performed an in-situ litter decomposition experiment in deciduous (Quercus variabilis ) and coniferous (Pinus massoniana ) forests with and without addition of the earthwormEisenia fetida in Eastern China. During one year, we measured litter mass loss, total carbon (C) and N loss, soil pH and soil microbial biomass. To better understand the pathways how the effect of earthworms on litter mass loss varies with different types of deposited compounds, we applied structural equation modelling. We hypothesized that (1) N, Na and PAHs addition all decrease litter mass loss; (2) the positive effect of earthworms on litter mass loss is significantly decreased by the addition of N, Na and PAHs, and (3) soil pH and microbial biomass as the modulators on litter mass loss are reduced by N, Na and PAHs addition, but enhanced by earthworm.
2 Materials and Methods