Litter decomposition and N release are the key processes that strongly determine the nutrient cycling at the soil–plant interface; however, how these processes are affected by grazing or grazing exclusion in the alpine grassland ecosystems on the Qinghai-Tibetan Plateau (QTP) is poorly understood. So far few studies have simultaneously investigated the influence of both litter quality and incubation site on litter decomposition and N release. Moreover, previous studies on the QTP investigating how grazing exclusion influences plant abundance and biodiversity usually lasted for many years, and the short-term effects have rarely been reported. This work studied the short-term (6 months) effects of grazing and grazing exclusion on plant community composition (i.e., plant species presented) and litter quality and long-term (27–33 months) effects on soil chemical characteristics and mixed litter decomposition and N release on the QTP. Our results demonstrate that (1) shorter-term grazing exclusion had no effect on plant community composition but increased plant palatability and total litter biomass; (2) grazing resulted in higher N and C content in litter; and (3) grazing accelerated litter decomposition, while grazing exclusion promoted N release from litter and increased soil organic carbon. In addition, incubation site had significantly more impact than litter quality on litter decomposition and N release, while litter quality affected decomposition in the early stages. This study provides insights into the mechanisms behind the nutrient cycling in alpine ecosystems. We suggest that periodic grazing and grazing exclusion is beneficial in grassland management on the QTP.
The Qinghai-Tibetan Plateau (QTP) represents an important ecoregion in China (Wen et al., 2010), in which alpine grasslands cover more than 85 % of total area and are regarded as the major land unit of natural pastures in China (Dong et al., 2010). However, the grassland systems in this region have suffered from severe degradation driven by a range of factors including climate change, overgrazing, overcultivation and poor management (Han et al., 2008; Li et al., 2009; Wu et al., 2009, 2010; Feng et al., 2010), and the degraded land area has been increasing at 1.2–7.44 % per year (Ma et al., 2007). Since the 1990s, the restoration of degraded grasslands has attracted considerable attention (Kang et al., 2007; Han et al., 2008), and some efforts have recently been directed towards grassland restoration and maintenance by increasing aboveground plant abundance (Niu et al., 2009) and biodiversity (Wu et al., 2009; Niu et al., 2010) and improving soil organic matter content and nutrient availability (Cao et al., 2004; Wu et al., 2010; Sun et al., 2011). It is well known that grazing may change the vegetation community structure, soil structure and nutrient cycling processes, and that such changes have important consequential impacts on the structure and functioning of the ecosystem as a whole. However, litter decomposition and N release, the key factors regulating the nutrient cycle and availability at the soil–plant interface through grazing (Carrera and Bertiller, 2013), are as yet little studied in these alpine ecosystems (Luo et al., 2010; Zhu et al., 2016).
Herbivore grazing may induce short-term ecophysiological changes in plant tissues, which in turn may translate into litter quality changes and long-term shifts in plant community composition. At the short-term ecophysiological level, grazing may promote the plant species producing high-quality litter (Holland and Detling, 1990; Sirotnak and Huntly, 2000; Olofsson and Oksanen, 2002; Semmartin et al., 2004, 2008) because the consuming of plant tissues by herbivores may favor the grazed species with a higher re-growth rate and greater nutrient contents in plant tissues due to the higher nutrient uptake (see Holland and Detling, 1990; Olofsson and Oksanen, 2002; Semmartin et al., 2008). At the long-term community level, selective foliar grazing may alter the competitive interactions and recruitment patterns of plant species, which may change their abundance and life-form structure (Bardgett and Wardle, 2003; Semmartin et al., 2008; Wu et al., 2009; Niu et al., 2010). For instance, herbivores preferentially feed on the most palatable plants (e.g., species with high nutrient and low fibre contents), which may promote dominance of unpalatable species (Garibaldi et al., 2007), resulting in the high inputs of low-quality litter to soil and thus a reduction of decomposition rate, nutrient availability and nutrient cycling (Ritchie and Knops, 1998; Moretto et al., 2001; Olofsson and Oksanen, 2002). Therefore, litter in grassland subject to long-term grazing may decompose more slowly. However, some studies demonstrate that grazing per se may accelerate litter decomposition by modifying site conditions for litter turnover through physical changes in the soil by herbivore activities, such as trampling and urine/dung deposition (Takar et al., 1990; Fahnestock and Knapp, 1994; Semmartin et al., 2008; Luo et al., 2010; Liang et al., 2018). Empirical evidence of variance in litter quality input and decomposition caused by grazing is still subject to debate (Garibaldi et al., 2007).
It is often assumed that higher nutrient content in plant tissue usually
results in faster litter decomposition and in higher nutrient
mineralization and availability in soil (Olofsson and Oksanen, 2002). At the
ecosystem scale, the chemical characteristics of plant litter, for example
the carbon
In addition to litter quality (its chemical composition), two further factors controlling litter decomposition are the climate (mainly temperature and humidity) and decomposing organisms (their abundance and activity) (Coûteaux et al., 1995; Aerts, 1997; Semmartin et al., 2004; Keeler et al., 2009; Berg and McClaugherty, 2014; Zhu et al., 2016). Climate usually regulates decomposition processes at global and regional scales (Coûteaux et al., 1995; Silver and Ryan, 2001), but microbial activity regulates decomposition processes through soil temperature and moisture effects (modified by grazing) at a local scale (Coûteaux et al., 1995; De Santo et al., 1993; Luo et al., 2010; Orsborne and Macauley, 1988). Generally, climatic influence dominates litter quality and decomposer activity in areas where weather conditions are unfavorable (Coûteaux et al., 1995), due to the dependence of decomposer activity on microclimate (De Santo et al., 1993). Under favorable conditions, litter quality may largely prevail as the regulator and remain important until the late decomposition stages (Coûteaux et al., 1995). However, specific temperature and moisture conditions and litter quality may interact strongly and thus the rate of litter decomposition is difficult to predict.
Most studies evaluating the effect of grazing on litter decomposition
usually focus on forest, grassland or crop ecosystems in temperate areas
(e.g., Aber and Melillo, 1980; Berg and Staaf, 1981; Luo et al., 2010;
McCurdy et al., 2013), largely ignoring those in the alpine zones. On the
QTP, previous studies prove that long-term grazing exclusion (
This study site was an alpine meadow on the eastern QTP, SW China
(33
The grassland selected for experiments was
To measure the annual litter composition and determine whether plants could
recover without grazing, three grazing (GP, 100
To measure the litter composition, litter of different species collected
from each quarter was identified. After litter species identification,
litter was separated into two groups of contrasting palatability to the
Tibetan sheep (Niu et al., 2009, 2010; Wu et al., 2009; see Supplement
Table S1): (1) palatable species – preferred and desirable species, and (2) unpalatable species –
undesirable and toxic species. To measure the dry
biomass, the palatable and unpalatable litter was separately oven-dried at
60
To measure the quality of litter collected from GP (GP-litter treatment) or
from GEP (GEP-litter treatment), the palatable and unpalatable litter from a
quarter was mixed again, then ground and stored in a ziplock bag with
10
We also examined the effects of grazing and grazing exclusion on soil
characteristics. We randomly collected five soil samples in each
experimental paddock (
In this experiment, we included four treatments: (1) GP-GP, litter of all species was collected from and incubated in the GP; (2) GEP-GEP, litter of all species was collected from and incubated in the GEP; (3) GP-GEP, litter of all species was collected from the GP but incubated in the GEP; (4) GEP-GP, litter of all species was collected from the GEP but incubated in the GP. Treatments 1 and 2 were designated “in situ” incubation treatments, while treatments 3 and 4 were designated “across” grazing category incubation treatments, and these were included to improve understanding of the “home-field advantage” effect on litter deposition (John et al., 2011).
For each sample soil particles attached to the litter were cleaned off with
a soft brush, and samples were air-dried for 3 days. Dry litter
collected from each quadrat was cut to
Initial chemical characteristics (mean
Mean (
Mean (
A goodness-of-fit test (Shapiro–Wilk test, univariate procedure) was used to
test the normality of data before mean comparison using analysis of
variance (ANOVA, GLM procedure). All data were normally distributed. Data on
the initial chemical characteristics of litter (Table 1) were analyzed using
ANOVA followed by Tukey's Studentized multiple range test. Data on the
biomass of palatable or unpalatable species and those on the total biomass
between GP and GEP were also analyzed using ANOVA, while for GP or GEP the
difference in litter biomass between the palatable and unpalatable species
was compared using a paired-
Litter decay rate (
The decomposition rate (
Contribution (%) of incubation site (site: GP, grazing paddocks; GEP, grazing exclusion paddocks) and litter quality (quality: GP litter, mixed litter collected from grazing paddocks; GEP litter, mixed litter collected from grazing exclusion paddocks) to litter decomposition and N release.
A multivariate regression model (GLM procedure) employed by Vaieretti et al. (2013)
was applied to quantify the effect of incubation site and litter
quality (the two independent factors) on the final litter decomposition or N
release (the dependent factor) (Table 3): litter decomposition or N release
Dynamics (mean
Percentage of litter mass
There were 55 plant species (mostly forbs and grasses along with several legumes and
sedges) identified, and all were found in both GP and GEP, except
GP litter had significantly higher C and N but significantly lower
hemicellulose and hemicellulose
The concentrations of soil TN and TP were not significantly different
between the GP and GE for any year (LSD
The proportion of litter biomass remaining continuously decreased with
incubation duration, and litter decomposed faster in the first year (i.e.,
44.6, 38.5, 41.46 and 31.6 % decomposition in GP-GP, GEP-GEP, GEP-GP and
GP-GEP, respectively) than in the second year (i.e., 18.8, 24.1, 27.6 and
23.4 % decomposition in GP-GP, GEP-GEP, GEP-GP and GP-GEP, respectively)
(Fig. 3a). As shown in Table 2, the decomposition rate (
Generally, the percentage of total N release did not change during the first
winter when temperature was
The multivariate regression model indicates that both incubation site and
litter quality significantly affected litter decomposition and N release
(Table 3). Incubation site contributed respectively near 25 and 50 %
more to litter decomposition and N release than litter quality (Table 3).
Furthermore, the model predicts that GP resulted in significantly
greater litter decomposition (8.13 %) but significantly lower N release
(9.73 %) than did GEP (
A significant interaction between incubation site and litter quality for
litter decomposition was found (
Grazing or grazing exclusion of herbivores may indirectly alter the species
composition and functioning of grasslands by inducing shifts in plant
competitive interactions and recruitment patterns and thus changes in
species abundance and life-form structure (Bardgett and Wardle, 2003;
Garibaldi et al., 2007; Semmartin et al., 2008; Wu et al., 2009; Niu et al.,
2010; Chaneton, 2011). However, our results indicate that herbivore grazing
or grazing exclusion did not alter plant community composition in terms of
species inventory, as species found in the GEP mostly also occurred in the
GP. On the QTP, species composition is grazing intensity dependent (Niu et
al., 2010; Sun et al., 2011) and/or grazing
exclusion period dependant (Wu et al., 2009). Thus our results imply that a
stocking rate of 4 Tibetan sheep ha
However, our results show that herbivore grazing significantly altered species composition in terms of species abundance or palatability, with significantly less palatable as well as total litter produced in the GP compared to the GEP (Fig. 1). The low biomass of palatable species in GP may be attributed to the more palatable species (mostly the grasses and sedges; see Supplement Table S1) on the QTP being taller (Sun et al., 2011), and therefore more accessible to herbivore grazing, in addition to being more likely to be grazed by preferential grazing. Through these two mechanisms, the biomass of palatable species in the GP would subsequently be reduced. Results of this study indicate that grazing exclusion for a short period may allow the recovery of palatable species in the alpine meadows. However, there was no significant difference in the litter biomass of unpalatable species between the GP and GEP (Fig. 1), which provides evidence against the assumption that removing the canopy of palatable species may allow intra- and inter-specific competition for light, which ultimately favors the establishment of short, less-palatable species (Sternberg et al., 2000; Pavlů et al., 2008; Wu et al., 2009; Sun et al., 2011).
It is generally accepted that litter quality is usually determined by the
levels of various chemical compounds such as soluble C, N and P, as well as
lignin or lignin
For a given climatic region, the ecological processes of litter
decomposition are regulated by incubation microenvironment (i.e.,
grazing and grazing exclusion and soil property in this study) and litter
quality. Our results suggest that herbivore grazing played a major role in
litter decomposition on the QTP. Many studies have demonstrated that litter
quality is one of the most important factors affecting the litter
decomposition, and litter with higher N content but lower lignin and
lignin
Additionally, incubation site had a significantly greater effect on litter
decomposition (
In a long-term (9 years) study on the QTP, Wu et al. (2009) reported that grazing exclusion favors the increase in soil TN, soil organic matter, SOC, soil microbial biomass carbon and soil carbon storage. It is interesting that in the present study, only SOC significantly increased after 3 years of grazing exclusion (Fig. 2). The increase in SOC in GEP may be because grazing exclusion prevents the reduction of removal of palatable litter by the herbivores (Fig. 1), and the organic C locked within plant tissues may be returned to the soil during litter decomposition instead (Bardgett and Wardle, 2003; Wu et al., 2009). Holland and Detling (1990) and Ågren et al. (1999) stated that increasing carbon availability in soil may promote decomposer growth and activity even at low nitrogen concentrations. However, the expected results, i.e., significantly higher litter decomposition rate caused by the possible increasing decomposer mass and/or activity in the grazing exclusion grasslands (Wu et al., 2009), were not observed in the GEP in this study (Table 2, Fig. 4a). Thus, soil properties are unlikely to be significantly changed through grazing or grazing exclusion over relatively short periods, indicating that limited grazing events have a smaller effect on litter decomposition under cool environments on the QTP than in experiments conducted in warmer climates.
N release is a more complex process compared to litter decomposition. N
release may involve any one or both processes of N immobilization and N
mineralization, where the former results in the accumulation of N in the
litter and the latter causes the release of N from the litter (Manzoni et
al., 2008). Swift et al. (1979) and Berg and McClaugherty (2014) reported
that the biological decomposition of litter is mainly carried out by
microbial decomposers, which per se have a higher N
It is not surprising that because both litter decomposition and N release
are regulated by decomposers synchronously, incubation site also had a
significantly greater effect (
Results of our study are not completely consistent with previously proposed
hypotheses. On the cold QTP, short-term grazing exclusion did not promote
species abundance but increased plant palatability and total litter biomass.
Grazing improves litter quality through higher N content but lower
hemicellulose and hemicellulose
Data are available from the author, Fujiang Hou (cyhoufj@lzu.edu.cn), upon request.
The supplement related to this article is available online at:
YS and FH designed and FH supervised the experiments. YS, FH, ZW and SC performed research and collected data. XH, FH and YS analyzed data and prepared the manuscript, and all authors contributed to the writing.
The authors declare that they have no conflict of interest.
We are very grateful to Jens-Arne Subke (editor) and two anonymous reviewers for their constructive comments and suggestions, which have significantly improved the paper. We are also grateful to Cory Matthew for his valuable comments and time spent editing the English of a previous version of the paper. This study was financially supported by the National Key Project of Scientific and Technical Supporting Programs (2014CB138706), National Natural Science Foundation of China (no. 31672472), Program for Changjiang Scholars and Innovative Research Team in University (IRT_17R50) and the independent grants from the State Key Laboratory of Grassland Agro-ecosystems (SKLGAE201708). Edited by: Jens-Arne Subke Reviewed by: two anonymous referees