Varying soil respiration under long-term warming and clipping due to shifting carbon allocation toward below-ground
Introduction
Soil respiration (Rs) is the second largest carbon (C) flux in terrestrial ecosystem (Ben and Allison, 2010; Raich and Potter, 1995; Unwin, 1997), releasing nearly one twelfth of carbon dioxide (CO2) stock from the soil surface to the atmosphere through microbe and root respiration (Kristiina et al., 2014). As soil organic C content (1500 – 2400 Pg C) is over three times larger than atmosphere (589 – 750 Pg C) or plant biomass (450 – 650 Pg C) (Carvalhais et al., 2014; Lal, 2004; Pries et al., 2017), even a small change in Rs has considerable impacts on atmosphere CO2 concentration and terrestrial C-climate feedbacks (Jenkinson et al., 1991; Schimel et al., 1994). Although many filed experiments (Bronson et al., 2008; Carey et al., 2016; Luo et al., 2009; Luo et al., 2001) and modeling analyses (Friedlingstein et al., 2006; Jones et al., 2005; Raich et al., 2002) showed that Rs changes substantially with warming, the mechanisms underlying its responses are not well understood (Jones et al., 2003; Trumbore, 2010), especially for the responses of Rs components: autotrophic respiration (Ra, respiration of root, mycorrhizal and rhizosphere) and heterotrophic respiration (Rh, microbial decomposition of plant and soil organic matter) (Wang et al., 2019a).
Although partitioning Rs into Ra and Rh has received considerable attention, it is still a challenge to quantify these two processes under global climate change (Baggs, 2006). It has been reported that Rh is more sensitive to warming than Ra (Lin et al., 2001), while other study showed opposite result (Zhou et al., 2007). Furthermore, previous studies also reported that the response of Rs to temperature is controlled more by Ra than Rh (Lavigne et al., 2003) or Ra and Rh respond equally to temperature increase (Noh et al., 2017). As Ra and Rh have shown different responses to warming, understanding the differential controls of Ra and Rh would help to reveal the mechanisms underlying Rs in response and feedback to global warming (Zhou et al., 2010).
Soil respiration in response to warming varies largely across years. Warming initially stimulates Rs by enhancing decomposition (Lloyd and Taylor, 1994). However, the depletion of labile C in soil under higher microbial activity (Bradford et al., 2008; Eliasson et al., 2005) dampens the stimulation effect (Contosta et al., 2015), which means short-term (<3 years) responses of ecosystems and its processes to warming always differ from long-term (>3 years) responses (Bradford et al., 2008; Wang et al., 2019b). For example, long-term warming increases Rs (Pries et al., 2015), whereas Rs shows a neutral (Li et al., 2013), negative (Reynolds et al., 2015) or positive (Zhou et al., 2016) response to short-term warming in different ecosystems. Therefore, studies of long-term experiments are necessary to understand the responses of soil respiration and its components to global warming.
In grassland ecosystems, the responses of soil respiration to warming were always confounded with human disturbance, such as mowing or clipping for hay (Luo et al., 2009; Niu et al., 2013). Clipping substantially affects ecosystem C fluxes of grassland (Bahn et al., 2006) through influencing soil microclimate (Luo et al., 2010), photosynthetic activity (Anten and Ackerly, 2001) and nutrient cycling (Ross et al., 1999). Since soil temperature is usually higher and soil moisture is lower under warming and clipping than that under warming or clipping treatment alone, soil respiration is expected to change more under warming plus clipping treatment (Xu et al., 2014). However, a previous study has reported that clipping significantly enhances ecosystem C fluxes, but it does not significantly interact with warming in a tallgrass prairie ecosystem (Niu et al., 2013), suggesting that the effect of warming and clipping on ecosystem C fluxes are statistically independent. In addition, no interaction between warming and clipping was found in a 3-year experiment conducted in Tibetan plateau (Lin et al., 2011). On contrary, a field experiment conducted in Great Plain Apiaries suggested that warming and clipping interacted to affect soil microbial community interactively (Zhou et al., 2006). These contradictory results are probably due to that the responses of soil CO2 fluxes to warming and clipping depend on hydrological variations (Peng et al., 2014), precipitation distribution and summer severe drought (Zhou et al., 2007). Therefore, how warming interacts with clipping in changing soil respiration and its components remains highly uncertain.
Warming induced changes in net primary productivity (NPP), either positive (Rustad et al., 2001) or negative (Wu et al., 2011), is considered an important cause for soil respiration responses. For example, warming induced decrease in NPP reduces Ra and Rh through a decrease in the supply of photosynthate (BhupinderpalSingh et al., 2003). Below-ground net primary productivity (BNPP), which is more sensitive to warming than above-ground net primary productivity (ANPP) (Xu et al., 2012), represents more than half of primary productions in grasslands and plays an important role in providing organic matter to soil (Luo et al., 2009). Moreover, the ratio of ANPP to BNPP (A/B) is a central issue in plant ecology and evolution, which shows the strategy of plants or ecosystems to partition photosynthate in above-ground versus below-ground tissues (Vogt et al., 1998) under global climate change (McCarthy and Enquist, 2007). Understanding A/B dynamics is pivotal to improving our knowledge of C allocation and the driving factors in Rs. To date, however, little work has been devoted to exploring how the response of soil respiration and its components to warming relates to the C allocation, especially from long-term field experiments.
Qinghai-Tibet Plateau warms more rapidly than the global average and also is one of the most sensitive ecosystems to global climate change (Crowther et al., 2016; Ma et al., 2018). Grazing or clipping for hay harvest is the most prevalent land-use pattern in this region. However, the response of soil respiration and its components under both global warming and clipping has received less attention due to the tough environmental conditions in this ecosystem. In this study, we conducted a six-year warming and clipping field experiment in an alpine meadow ecosystem on the Qinghai-Tibet Plateau. The specific questions we addressed are (1) how climate warming interacts with clipping to change soil respiration and its components? (2) how the responses of soil respiration and its components change with years? and (3) how C allocation changes and relates to the responses of soil respiration and its components under long-term warming? Accordingly, we hypothesized that (1) clipping stimulates warming impact on soil respiration and its components, (2) long-term warming stimulates soil respiration and its components but the responses vary largely over years, and (3) changes in C allocation contribute to the responses of soil respiration.
Section snippets
Study site
The study was conducted in an alpine meadow on the eastern edge of Qinghai-Tibetan Plateau (32°48′N, 102°33′E), which is located in Hongyuan County, Sichuan province of China, at a mean altitude around 3500 m. The average annual precipitation is approximately 753 mm (1961-2013), of which more than 80% occurs during May to September, and the mean annual evaporation is 684.2 mm. The site belong to continental monsoon climate, with a mean annual temperature of 1.5°C, while winters are severe and
Soil microclimate
Warming significantly increased soil temperature (ST; P < 0.001), whereas the main effects of clipping showed no significant effect on ST (Table 1). The warming treatments W1.5 and W2.5 increased ST by an average of 1.56°C and 2.34°C, respectively, in the no clipping plots and by 1.69°C and 2.39°C, respectively, in the clipping plots at the depth of 10 cm in comparing with the control (P < 0.001; Fig. 1). Soil moisture (SM) was reduced by an average of 2.49% and 4.93% with W1.5 and W2.5
Discussion
Based on a 6-year experiment investigating the response of soil respiration and its components to warming and clipping, this study indicated that Rh and Ra had different sensitivities to warming, with Rh decreasing whereas Ra increasing with warming, leading to no significant impacts on Rs. Clipping significantly stimulated Rs, Rh and Ra as well as their responses to warming. Interestingly, warming effect varied largely with years, which was due to the changes in the ratio of ANPP to BNPP and
Declaration of Competing Interest
The authors declare no competing financial interests.
Acknowledgements
The authors thank the staff of Institute of Qinghai-Tibetan Plateau in Southwest University for Nationalities. This study was financially supported by the National Natural Science Foundation of China (31988102, 31625006), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDA23080302).
References (67)
- et al.
Soil microbial communities vary as much over time as with chronic warming and nitrogen additions
Soil Biol. Biochem.
(2015) - et al.
Responses of soil respiration and its components to experimental warming in an alpine scrub ecosystem on the eastern Qinghai-Tibet Plateau
Sci. Total Environ.
(2018) - et al.
Different responses of soil, heterotrophic and autotrophic respirations to a 4-year soil warming experiment in a cool-temperate deciduous broadleaved forest in central Japan
Agricult. For. Meteorol.
(2017) - et al.
Soil microbes and their response to experimental warming over time: A meta-analysis of field studies
Soil Biol. Biochem.
(2017) - et al.
Land-use change: effects on soil carbon, nitrogen and phosphorus pools and fluxes in three adjacent ecosystems
Soil Biol. Biochem.
(1999) - et al.
Canopy-level photosynthetic compensation after defoliation in a tropical understorey palm
Functional Ecology
(2001) Partitioning the components of soil respiration: a research challenge
Plant Soil
(2006)- et al.
Root respiration in temperate mountain grasslands differing in land use
Global Change Biol.
(2006) Effects of Soil Temperature and Moisture on Soil Respiration on the Tibetan Plateau
PLoS One
(2016)- et al.
Temperature-associated increases in the global soil respiration record
Nature
(2010)
Tree root and soil heterotrophic respiration as revealed by girdling of boreal Scots pine forest: extending observations beyond the first year
Plant Cell and Environment
Thermal adaptation of soil microbial respiration to elevated temperature
Ecology Letters
Response of soil surface CO2 flux in a boreal forest to ecosystem warming
Global Change Biol.
Temperature response of soil respiration largely unaltered with experimental warming
PNAS
Global covariation of carbon turnover times with climate in terrestrial ecosystems
Nature
Quantifying global soil carbon losses in response to warming
Nature
Simple additive effects are rare: a quantitative review of plant biomass and soil process responses to combined manipulations of CO2 and temperature
Global Change Biol.
Accumulation of soil carbon under elevated CO2 unaffected by warming and drought
Global Change Biol.
The response of heterotrophic CO2 flux to soil warming
Global Change Biol.
Enhanced decomposition of stable soil organic carbon and microbial catabolic potentials by long-term field warming
Global Change Biol.
Climate-carbon cycle feedback analysis: Results from the (CMIP)-M-4 model intercomparison
J. Climate
Separating root and soil microbial contributions to soil respiration: A review of methods and observations
Biogeochemistry
Geographical and interannual variability in biomass partitioning in grassland ecosystems: a synthesis of field data
New Phytol.
Model estimates of CO2 emissions from soil in response to global warming
Nature
Global climate change and soil carbon stocks; predictions from two contrasting models for the turnover of organic carbon in soil
Global Change Biol.
Uncertainty in climate-carbon-cycle projections associated with the sensitivity of soil respiration to temperature
Tellus Series B-Chemical and Physical Meteorology
Temperature sensitivity of soil respiration rates enhanced by microbial community response
Nature
Soil carbon sequestration impacts on global climate change and food security
Science
Soil respiration responses to temperature are controlled more by roots than by decomposition in balsam fir ecosystems
Can. J. For. Res.-Revue Canadienne De Recherche Forestiere,
Contrasting responses of heterotrophic and autotrophic respiration to experimental warming in a winter annual-dominated prairie
Global Change Biol.
Contrasting responses of heterotrophic and autotrophic respiration to experimental warming in a winter annual-dominated prairie
Global Change Biol.
Time-dependent responses of soil CO2 efflux components to elevated atmospheric CO2 and temperature in experimental forest mesocosms
Plant Soil
Cited by (16)
Individual and interactive effects of air warming and elevated O<inf>3</inf> on carbon fixation and allocation in two urban tree species
2024, Agricultural and Forest MeteorologyShort-term warming-induced increase in non-microbial carbon emissions from semiarid abandoned farmland soils
2023, Global Ecology and ConservationClipping increases ecosystem carbon use efficiency by decreasing the dominance of grasses
2023, Agricultural and Forest MeteorologyIncreased plant growth may offset soil carbon loss caused by warming in an alpine Sibiraea angustata shrub ecosystem on the eastern Qinghai-Tibet Plateau
2022, Ecological IndicatorsCitation Excerpt :In addition, warming can alter the vertical distributions of alpine plant roots in soil profiles, influencing soil labile C inputs through root turnover and exudates; and thus affecting soil C storage at different soil depths (Sistla et al., 2013; Yuan et al., 2021b). For example, warming may increase the downward transport of root biomass and C allocation to deeper soil layers in alpine meadows and shrublands (Anadon-Rosell et al., 2014; Xu et al., 2016; Yan et al., 2021). Such changes in the nature and location of C inputs caused by warming will alter the activity of soil microbial decomposers and thereby influence soil C processes in soil profiles further (Sistla et al., 2013).
Biocrusts as a nature-based strategy (NbS) improve soil carbon and nitrogen stocks and maize productivity in semiarid environment
2022, Agricultural Water ManagementCitation Excerpt :The data demonstrated a time-dependent dynamics of carbon mineralization amount and its rate in response to the BSC addition. To sum up, biocrust mulching can elevate soil carbon level and the MBC & MBN concentration while lowering C/N ratio through regulating microorganism activities and cumulative CO2 release (Yan et al., 2021). Soil nitrogen is a key element in the nitrogen cycle and mobilization.