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